Kari Et Al. - 2019 - Orobanche Menace in Crop Plants Host Resistance A

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Biology and Management of Weedy

Root Parasites
D. M. Joel, J. Hershenhorn, H. Eizenberg, and R. Aly
Agricultural Research Organization
Newe Ya’ar Research Center
Ramat Yishay, Israel
G. Ejeta and P. J. Rich

Purdue University
Department of Agronomy
915 W. State Street
West Lafayette, Indiana 47907-2054, USA
J. K. Ransom
North Dakota State University
Department of Plant Sciences
P.O. Box 5051
Fargo, North Dakota 58105-5051 USA
J. Sauerborn
University of Hohenheim
Institute for Plant Production and Agroecology in the Tropics and
Subtropics
70593 Stuttgart, Germany
D. Rubiales
Institute of Sustainable Agriculture—CSIC
Alameda del Obispo s/n
Apdo 4084
E-14080 Córdoba, Spain
Horticultural Reviews, Volume 33. Edited by Jules Janick

© 2007 John Wiley & Sons, Inc. ISBN 978-0-471-73214-3
267
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268 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

J. SAUERBORN, AND D. RUBIALES
I. INTRODUCTION
II. ECONOMIC IMPACT
A. Weedy Orobanche Species
1. Orobanche crenata Forsk
2. Orobanche aegyptiaca Pers
3. Orobanche ramosa L.
4. Orobanche foetida Poir
5. Orobanche minor Sm
6. Orobanche cernua Loefl
7. Orobanche cumana Wallr
8. Orobanche coerulescens Stephan
B. Weedy Striga and Alectra Species
1. Striga spp.
2. Alectra vogelii Benth
III. DISTRIBUTION
IV. DEVELOPMENTAL ASPECTS
A. Seed Dormancy and After-Ripening
B. Wet Dormancy
C. Germination
1. Conditioning
2. Germination Stimulation
D. Haustorial Initiation
E. Attachment and Penetration
F. Further Haustorial Development
G. Host–Parasite Interaction
H. Seed Production and Dispersal
I. Host Resistance
1. Contribution of Basic Research
2. The Temperature Effect
J. Race Development
K. Diagnosis
1. Morphological Species Identification
2. Molecular Identification
V. MANAGEMENT
A. General Considerations
B. Orobanche Management
1. Chemical Control
2. Host Plant Resistance
3. Eliminating the Parasite Seed Bank
4. Biological Control
5. Artificial Resistance
6. Integrated Orobanche Management
C. Striga Management
1. Containment
2. Chemical Control
3. Host Plant Resistance
4. Cultural Management Practices
5. Biological Control
6. Integrated Striga Management
VI. CONCLUDING REMARKS
LITERATURE CITED
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4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 269
I. INTRODUCTION
Over 4000 species of angiosperms are able to directly invade and para-
sitize other plants (Nickrent et al. 1998), but only very few of them are
weedy and parasitize cultivated plants. Nevertheless, these weedy par-
asites pose a tremendous threat to world economy, mainly because they
are at present almost uncontrollable (Gressel et al. 2004; Parker and
Riches 1993). They belong to various plant families and attach to host
roots, shoots, or branches. Accordingly, we find mistletoes like
Arceuthobium that parasitize trees, climbers like Cuscuta that parasitize
shoots, and parasites like Striga and Orobanche that connect to host
roots. The latter plants are the weedy root parasites.
The most damaging weedy root parasites belong to the Orobanchaceae.
The broomrapes (Orobanche spp.) are widespread in Mediterranean
areas in Asia and Southern and Eastern Europe, attacking dicotyledo-
nous crops and depending entirely on their hosts for all nutritional
requirements. In tropical Africa, the most damaging parasitic weeds are
the witchweeds (Striga spp.), obligate root parasites of grain grasses and
legumes that endanger food supplies in many developing countries
(Parker and Riches 1993). Similar root parasites belonging to the genera
Alectra, Buchnera, and Rhamphicarpa attack agricultural crops in Africa
(Hoffmann et al. 1997; Kureh et al. 1995; Ouedraoga et al. 1999; Maiti
and Singh 2004), while Aeginetia attacked cereals and sugarcane in
Southeast Asia in the past. Currently, there is a single report from Ben-
gal, India on sugarcane infection with this parasite (B. R. Ray, pers.
commun).
The distinction between the two closely related families, Oroban-
chaceae and Scrophulariaceae has been demonstrated to be artificial,
based on molecular phylogenetic analysis (dePamphilis 1995). Thus, all
parasitic plants of these two families may be included in the Oroban-
chaceae. Accordingly, all agriculturally important root parasites of the
genera Striga, Alectra, Orobanche, and Aeginetia, can be included in the
same family.
Like other parasitic flowering plants, the root parasites develop a
haustorium that penetrates into host tissues and serves as a physiolog-
ical bridge that directly connects them to the vascular systems of their
hosts, allowing the uptake of water, nutrients, and assimilates. Some root
parasites, like Orobanche spp. and Aeginetia spp., completely lost pho-
tosynthetic capabilities, whereas other root parasites, like most species
within the genus Striga, are hemiparasites that retain photosynthetic
ability.
The weedy root parasites, which are often host specific, exert their
greatest damage prior to their emergence; therefore, the majority of field
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loss may occur before diagnosis of infection. In spite of intense efforts

during the 20th century, effective means to selectively control the vari-
ous species of parasitic weeds are still scarce or lacking. A wide variety
of approaches—physical, cultural, chemical, and biological—have been
explored against root parasites, but most of them are not effective, or not
selective to the majority of susceptible crops. This review summarizes
some major aspects of the biology of weedy root parasites and presents
an updated summary of the available knowledge concerning the means
for their management.
II. ECONOMIC IMPACT
Parasitic weeds develop a strong sink, which allows them to remove

water, minerals, and photosynthates from the crop. Thus, infection by
parasitic weeds reduces the ability of the hosts to grow and yield.

Over 20 Orobanche species have been described as weeds throughout
the world, and many are major weeds in Asian, European, and African
countries. This holoparasitic plant genus includes some of the most
devastating weeds in agriculture, particularly in Mediterranean climates,
with tremendous economic impact. The Latin name Orobanche is
derived from the Greek orobos, a vetch, and ancho, to strangle, referring
to the effect these parasites have on their hosts. The common name
“broomrape” ascribed to these weeds is a translation of medieval Latin
Rapum genistea, “broom knob”; rapum being a knob (or tubercle, i.e.,
the young parasite) formed on the roots of broom (Genista sp.) that is a
common host of O. majus in Europe. A few Orobanche species cause
severe damage in many important crops and so far there are only lim-
ited ways of control. Orobanche weeds are obligate root parasites that
attack roots of dicotyledonous plants. Unlike the Striga species, which
are usually rather selective in their host preference, some Orobanche
species are less selective and may attack a variety of host crops belong-
ing to various families.
1. Orobanche crenata Forsk. This parasitic weed, mainly restricted to

the Mediterranean basin, Southern Europe, and the Middle East, is an
important pest in grain and forage legumes, as well as in some Apiaceous
crops such as carrot (Daucus carota L.) and celery (Apium graveolens
L.) (Plate 4.1C, 4.2C,G). Sauerborn (1991) estimated that over one mil-
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lion hectares of faba bean in the Mediterranean region and western Asia
are infested or at risk from O. crenata. Yield loss by this species can be
severe. In carrot, Orobanche infection may lead to a 70% reduction in
sugar content (Schaffer et al. 1991). With legumes, the situation may be
even worse, and O. crenata infection may lead to the complete loss of
both garden and field pea (Pisum sativum L.) (Rubiales et al. 2006b).
Losses up to 95% were also reported for faba bean (Vicia faba L.) (Mesa-
García and García-Torres 1985) and lentil (Lens culinaris Medik.) (Sauer-
born 1991) depending on the infestation level and the planting date.
Thus, this species is known to devastate the legumes that serve as an
important source of protein in many Middle Eastern societies (Parker
and Riches 1993).
2. Orobanche aegyptiaca Pers. This species is an important pest of

many crops in Mediterranean countries in the Middle East and Africa,
extending eastward to central Asia, India, China, and southern Russia.
Orobanche aegyptiaca attacks crop plants belonging to various families,
including Asteraceae, Brassicaceae, Cucurbitaceae, Fabaceae, and
Solanaceae (Plate 4.1A, 4.2A,F). It attacks tomato (Lycopersicon escu-
lentum Mill.), potato (Solanum tuberosum L.), tobacco (Nicotiana spp.),
cabbage (Brassica spp.), oilseed rape (Brassica napus L.), sunflower
(Helianthus annuus L.), parsley (Petroselinum crispum (Mill.) Nym.ex
A.W.Hill), watermelon (Citrullus lanatus (Thunb.) Matsum. et Nakai),
faba bean, common vetch (Vicia sativa L.), chickpea (Cicer arietinum L.),
and lentil, and can also severely attack peanut (Arachis hypogaea L.)
(Parker and Riches 1993). Infestation of tomato and potato fields by O.
aegyptiaca is especially dangerous, as these crops prove highly suscep-
tible to Orobanche infection. Attempts to resume growing a susceptible
crop on infested land within decades are liable to result in immediate
re-infestation.
Extreme cases were documented in Israel, where O. aegyptiaca seeds
survived in soil for more than 40 years. In these cases, farmers planted
fruit trees, which are not attacked by Orobanche in Orobanche-infested
fields in order to escape damage. The newly planted tree orchards did
not show any Orobanche infection for decades, but once the trees were
cut, and vegetables were planted again in these fields, Orobanche imme-
diately occurred in dense populations, causing severe damage.
3. Orobanche ramosa L. This species attacks many different crop plants;

its host range resembles that of O. aegyptiaca. In early times, it was
known to attack cannabis (Cannabis sativa L.) and various solanaceous
crops, but currently its host range is very wide, and differs in the various
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countries. It attacks potato, tomato, eggplant (Solanum melongena L.),

and tobacco. It also severely attacks brassicas, melon (Cucumis melo L.),
watermelon, and cucumber (Cucumis sativus L.), and to a lesser extent
it may case damage to parsley, celery, parsnip (Pastinaca sativa L.),
some legumes, and lettuce (Lactuca sativa L.) (Plate 4.1E).
4. Orobanche foetida Poir. This parasitic weed has recently been

described to severely attack legumes in North Africa with yield losses
ranging 65 to 80%. O. foetida seems to be more aggressive on faba bean
and on common vetch than on other legumes (Plate 4.1B). Of the cool-
season grain legumes, only pea escapes its attack. Infection by this
species has also been reported in Tunisia on chickpea, sweet pea (Lath-
yrus odoratus L.), grass pea (L. sativus L.), berseem (Trifolium alexan-
drinum L.), barrel medic (Medicago truncatula Gaertn.), and
subterranean vetch (V. sativa ssp. amphicarpa (Dorthes) Asch. &
Graebn.) (Rubiales et al. 2006b).
5. Orobanche minor Sm. This species has a wide host range among for-
age legumes in temperate climates. Though known as a nonimportant
weed in most regions, including Australia, Japan, and Europe, it has
recently become a serious problem on red clover (Trifolium pratense L.)
in Oregon, US (Eizenberg et al. 2005b) (Plate 4.1D, Plate 4.2D).
6. Orobanche cernua Loefl. This parasitic weed is known in native habi-

tats to parasitize members of the Asteraceae, but as a weed it is typically
attacking solanaceous crops, mainly tobacco, tomato, and potato (Plate
4.1F).
7. Orobanche cumana Wallr. This species has specialized as a pest of

sunflower (Helianthus annuus L.) and is an increasing problem in
Mediterranean countries and Eastern Europe. It was supposed to have
evolved from O. cernua when sunflower started to play an economic role
in Russia in the 19th century, but both morphological and molecular dif-
ferences support the assumption that this is a solid species. Sunflower,
an important source of oil, is in danger due to severe infestation by this
parasite in several million hectares throughout eastern and Southern
Europe and in Asian countries including China. Confectionary sun-
flower is also affected, and seems to be even more susceptible to this par-
asite (Plate 4.1G, Plate 4.2E). Heavily infested fields may not give any
yield at all.
8. Orobanche coerulescens Stephan. This parasitic species was reported

to attack sunflower in China, causing up to 20% loss in oil production.
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1. Striga spp. The economic impact of weedy Striga species is greatest
in cereals cultivated in Africa, e.g., pearl millet (Pennisetum glaucum L.),
sorghum (Sorghum bicolor (L.) Moench), and maize (Zea mays L.). The
most destructive species on cereals are S. hermonthica Del. Benth. (Plate
4.1J, 4.2H,I) and S. asiatica (L.) Kuntze (Plate 4.1J, K.2K,L). Second in
their economic impact in Africa are S. aspera Benth. and S. forbesii Benth.
(Parker and Riches 1993). Damage to crops by Striga is often severe. The
common name “witchweed” ascribed to these weeds befits the debili-
tating and “bewitching” effect they inflict on host plants even before they
emerge and become visible above ground. A striga is a blood-drinking
night spirit of classical antiquity that became known as a witch in folk-
lore. Striga species parasitize several important food crops like fonio
[Digitaria exilis (Kipp.) Stapf], finger millet [Eleusine coracana (L.)
Gaertn.], and rice (Oryza sativa L.) in much of Africa and some parts of
Asia (Musselman 1980).
Cereal and legume crops vulnerable to Striga are the major source of
energy and protein in the diets of hundreds of millions of people in the
semi-arid tropics. As crops of resource-poor households are affected by
these parasites, they impose an additional stress on farmers, who have
little capacity for investment in crop production, and have to cope in an
environment characterized by marginal rainfall for cropping, and declin-
ing soil fertility.
Striga may have already become the greatest biological constraint to
food production in these parts of Africa, probably even a more serious
agricultural problem than insects, birds, or plant diseases (Ejeta and But-
ler 1993). Striga has thus become a poor man’s problem in Africa.
Unlike most of the Striga species, the host range of S. gesnerioides
(Willd.) Vatke is restricted to dicotyledonous plants. It is an important pest
of Fabaceae, especially cowpea (Vigna unguiculata (L.) Walp) (Plate 4.1I).
Crop losses due to Striga infestation are usually high with range of
estimates varying depending on the crop cultivar and degree of infesta-
tion. Annual crop loss due to Striga infestation in Africa has been esti-
mated at 40% (Lagoke et al. 1991), but in some countries such as Sudan
and Ethiopia, greater losses of 65 to 100% have been frequently experi-
enced in the fields, resulting in repetitive crop failures. According to
FAO studies, over 100 million people lose half their crop production to
this flowering, root-attaching parasite (Berner et al. 1995). Striga spp. are
a major reason that maize yield in the 1.2 million ha sown in Sub-
Saharan Africa has dropped from near the world average of 4.2 t
(tones)/ha in the last few decades to the present 1.3 t/ha (Kanampiu et
al. 2002b).
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In the US, where both S. asiatica and S. gesnerioides have been unin-
tentionally introduced, infestation has been contained to a few pocket
areas in a couple of counties in the Carolinas, perhaps owing to an
aggressive control effort spearheaded by the United States Department
of Agriculture (USDA/APHIS) over the last three decades (Eplee and
Norris 1995). On the other hand, in many places in Africa and India,
Striga infestation has reached epidemic proportions and is presenting a
rather desperate situation to small subsistence agriculture. The Striga
problem in Africa is particularly increasing because the use of agricul-
tural inputs has been unaffordable, and population growth has forced
farmers to alter traditional methods of prolonged fallow and intercrop-
ping to meet growing demand on farm land and food production. In the
past, prolonged fallow and intercropping had helped to keep Striga
infestation at tolerable levels (Dogget 1984; Sauerborn et al. 2003). The
spread of Striga may increase further as farmers adopt improved crop
cultivars that tend to be less tolerant than the traditional ones that have
evolved with parasitic populations in the ecosystem.
2. Alectra vogelii Benth. This parasite causes considerable yield losses

of grain legume crops (Plate 4.1H), particularly cowpea, throughout
semiarid areas of sub-Saharan Africa (Parker and Riches 1993). Its main
hosts are cowpea in Southern, East, and West Africa and peanut in East
and West Africa. Soybean (Glycine max (L.) Merr.), bambara groundnut
(Vigna subterranea (L.) Verdc.), common bean (Phaseolus vulgaris L.),
mung bean (Vigna radiata (L.) Wilczek), and many legume fodder crops,
including hyacinth bean (Dolichos lablab L.), siratro (Macroptilium
atropurpureum (DC.) Urb.), and velvet bean (Mucuna pruriens (Stickm.)
DC.) are also parasitized (Riches 1989). Total crop loss in cowpea was
reported in extreme cases. 15% yield loss was observed in peanut in
Nigeria, 30 to 50% yield loss was observed in bambara, and late-sown
crops of soybean were completely destroyed by A. vogelii in northern
Nigeria (Rubiales et al. 2006b).
III. DISTRIBUTION

Orobanche is the largest genus among the holoparasitic members of
Orobanchaceae and comprises about 170 species distributed predomi-
nantly in the Northern Hemisphere (Schneeweiss et al. 2004). Only a few
species are weedy, but their impact on agriculture is tremendous. The
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geographical distribution of the weedy species of Orobanche is mainly

Mediterranean, but during recent decades they are spreading to other
areas due to seed movement by humans. The areas infested by the seven
important species of Orobanche are vast and ever-growing, because
farmers do not have the resources and the education needed for sanita-
tion measures in agricultural fields, and since quarantine services do not
have the means to monitor Orobanche seed in seed testing stations.
Nevertheless, sanitation measures are essential in order to limit
Orobanche distribution.
Orobanche crenata has its main area of distribution in the Mediter-
ranean-Middle East region and is particularly harmful in cool season
food legumes, such as faba bean and lentil, causing complete loss of
yield with severe infestations. Typically, there is a low genetic differ-
entiation among O. crenata populations in the Mediterranean area and
a considerably higher variation within each population that is consis-
tent with the predominantly allogamous behavior of O. crenata (Román
et al. 2002a). This species occurs exclusively in agricultural and dis-
turbed habitats, and is highly adapted to agricultural conditions. It is
characterized by large erect plants, branching only from their under-
ground tubercle. The spikes may reach the height of up to 1 m, bearing
many flowers of diverse pigmentation, from yellow, through white to
pink and violet.
The distribution of O. cumana coincides with that of sunflower fields
in Europe and Asia, ranging from Spain in the West to China in the East.
Being a relatively young weed, and with its rather autogamous nature,
this species shows a relatively low genetic variation, but due to the use
of a variety of resistant sunflower lines, it has developed a series of races
with various degrees of virulence (Melero-Vara et al. 2000; Antonova
1998). The plant is composed of a single upright stem that may reach 60
cm in height, bearing typically bent tubular flowers that are usually
pigmented in violet, apart from their base that remains white.
Orobanche aegyptiaca Pers. is an important pest of many crops in the
Eastern parts of the Mediterranean, in the Middle East and in parts of
Asia, while O. ramosa L. is more common as a weed in Europe, parts of
Africa and Asia, with some overlap with O. aegyptiaca in the northern
parts of the Middle East. These two species are very similar to each other,
with possible natural hybrids (Musselman 1986). However, O. aegypti-
aca is more aggressive and adapted to more arid regions, and therefore,
it seems to gradually replace O. ramosa in some countries, such as
Israel. With global heating we may anticipate further spread of O. aegyp-
tiaca. Orobanche ramosa has been introduced to the US, Cuba, Central
America, Chile, Australia, and South Africa. Unlike O. aegyptiaca,
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which is found only in cultivated and disturbed habitats, O. ramosa is

also known as a native plant in Europe, the Middle East and Asia. Both
species have branched stems with flowers that may significantly differ
in color, from white to dark blue. Differences may also be found in plant
size that may be highly branched and reaching 40 to 50 cm on well-
developed hosts, while in nonirrigated fields, they may be much smaller,
even 5 to 10 cm with only few flowers. O. ramosa may differ in mor-
phology in different countries, therefore, it is often divided into sub-
species, but they all are usually smaller than O. aegyptiaca and their
flowers more delicate and smaller. A simple feature that allows field dis-
tinction between O. ramosa and O. aegyptiaca is the hairiness of the sta-
mens between the two pairs of anther cells, which occurs only in O.
aegyptiaca.
Orobanche minor Sm. resembles O. crenata Forsk. in its stout,
unbranched stem, but it has smaller flowers, with smaller lips. It was
known in the past as an agricultural weed in Europe, but it is not com-
mon as such any more. It is found in native and disturbed habitats
throughout the central and southern parts of Europe, and extends to the
eastern coast of Africa and southward (Parker and Riches 1993). In addi-
tion, it was imported to various other parts of the world and is currently
found as a garden weed. In Australia, it is common in clover fields with-
out causing any significant damage, but recently it became a serious
problem on red clover fields in Oregon, US (Eizenberg et al. 2004a). The
species is highly diverse, and a number of subspecies are recognized in
Europe, together forming the O. minor group.
Orobanche foetida Poir. is known as a weed only in Northern Africa
(Tunisia and Morocco), but the species is also common in native habi-
tats in Spain and France. The plant has unbranched stems that bear red
or purple flowers that release an unpleasant smell.
Orobanche cernua Loefl. is common throughout the Old World,
mainly parasitizing perennial Asteraceae. It also grows on sandy coastal
soils in South Australia. The weedy O. cernua occurs in Southern
Europe, the Middle East and throughout Asia, including China. It attacks
various host plants, mainly of the Solanaceae. O. cernua develops
unbranched stems carrying rather small tubular flowers with short blue
teeth. O. cumana Wallr., which typically attacks sunflower, seems to
have evolved from O. cernua, but it is currently regarded a separate
species that is clearly distinct from the weedy O. cernua.

Striga spp. are native to the grasslands of the Old World and reach their
greatest diversity in Sub-Saharan Africa (Mohamed et al. 2001). The
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genus Striga includes 50 to 60 species, all of which are said to be para-

sitic, though only about a quarter parasitize crops. The rest grow on wild
hosts in ecosystems evolving for an estimated 40 million years (Raynal-
Roques 1996). However, the following four obligate parasitic species of
the genus Striga are recognized as the most economically important
because of their impact as yield reducers (Parker and Riches 1993):
Striga hermonthica Del. Benth. is widespread in Africa in the area
between 5° north and 20° south latitudes, though it is also found in Asia.
This species is broadly adapted to agricultural conditions and occurs
almost exclusively on crop hosts. It is characterized by large erect plants
(up to 50 to 100 cm high), spikes of many pink flowers, five ribs on the
calyx, and bracts below each flower fringed with hairs. As an obligate
outcrosser, its populations are diverse morphologically, as evidenced
mainly through the size of plants and shades of color of the flowers
(often various shades of pink, and even an occasional white flowered
plant appear in the same field). Striga hermonthica is parasitic to a
number of cereal crops in Africa and Arabia.
Striga asiatica (L.) Kuntze has well established morphotypes in dif-
ferent geographic regions. A major crop pest, though less broadly
adapted than S. hermonthica, it occurs more commonly on wild grasses.
Its flowers are white in India and deep red in the US, bright red in the
corolla and yellow on the undersurface in southern Africa, and yellow
or pale pink in Indonesia. Occasional yellow-flowered plants are
reported in red-flowered populations of S. asiatica in North Carolina,
Burkina Faso, and South Africa. This species is identified by 10 distinct
ribs on the calyx. Plants are slender with erect herbs, 15 to 30 cm in
height, hairy or glabrous and with glandular pubescent buds.
Striga forbesii Benth. is widespread in Africa and islands of the Indian
Ocean but predominantly found in the Southern Hemisphere with
greater expanse found in Zimbabwe, Tanzania, and Madagascar. Eco-
logically, it favors areas with relatively wet soil conditions. Plants of S.
forbesii are intermediate in size between S. asiatica and S. hermonth-
ica, often 30 to 40 cm high, and differ from both species in the shape of
the leaves. Flowers are large, comparable with those of S. hermonthica
but fewer, only 2 to 6 open at a time. Flower color is pale salmon-pink,
though an occasional white flower is also observed. As in S. asiatica, no
cross-pollination is required and flowers self-pollinate before opening.
S. forbesii is much more commonly seen on wild hosts, though it is also
parasitic to crop plants.
Striga gesnerioides (Willd.) Vatke is a small plant with a rather suc-
culent appearance and growing only up to 15 to 30 cm in height. The
plant is usually extensively branched from just below ground level.
Whole plants are often pale green or purplish with little chlorophyll.
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Leaves are reduced to scales ranging from 0.5 to 0.7 cm. long and often
appressed to the stem. Flowers are usually mauve/purple (range from
light pink to purple) though very rarely white or yellow flowers are also
spotted. The flowers appear showy with two or three flowers open on
each plant at peak of flowering but turn blue-black as they wither. Unlike
other Striga species, S. gesnerioides form a very large tuberous hausto-
rium that may reach up to 3 cm in diameter. Despite an extensive host
range, S. gesnerioides is of economic significance as a parasite of cow-
pea, tobacco, and sweetpotato (Ipomoea batatas (L.) Poir.).
Alectra vogelii Benth. plants are rather large, hairy, with a leafy
appearance, growing up to 30 to 45 cm. The plant is usually not
branched, but it may branch from near the ground level. Typically, the
underground stems are bright orange. The flower buds are enclosed in
a densely hairy calyx whose five lobes have a triangular tip with an
obtuse apex. The corolla is pale yellow, bell-shaped, 0.5 to 1.0 cm wide,
a little longer than the calyx. (Parker and Riches 1993). This species is
associated with cowpea fields throughout the semiarid areas of tropical
Africa, from South Africa, through central Africa to Mali, Burkina Faso,
and Kenya.
IV. DEVELOPMENTAL ASPECTS
Weedy root parasites of the Orobanchaceae exhibit two main life phases:
independent and parasitic (Joel et al. 1995b). The independent phase
begins with seed imbibition and germination and lasts a few days until
the germinated parasite finds a host and attaches to it. This life phase is
facilitated by consumption of material stored in the seed, mainly lipids.
The parasitic life phase, during which the parasite becomes dependent
on nutrients derived from the host, starts as soon as the haustorium
invades the host root, eventually forming a physiological bridge between
the vascular system of the host and that of the parasite (Joel 2000). The
life cycle is summarized in Fig. 4.1.
The seeds of obligate parasitic weeds are very small, approximately
0.20 to 0.35 mm long, and contain a reduced embryo that is composed
solely of a short radicle, without a plumule and cotyledons. When it ger-
minates, only a radicle emerges out of the tiny seed. The small storage
reserves, mainly composed of lipids, are capable of supporting a few
days of autonomous growth (Musselman 1980; Joel et al. 1995b; Bar Nun
and Mayer 2002). The emerging radicle grows to a limited extent (few
millimeters) and can therefore be seen only under the microscope. When
a root host is reached the radicle tip develops into an attachment organ,
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DRY SEED
Imbibition water
Conditioning
germination
Germination stimulants
SEEDLING
Attachment
Haustorium penetration
TUBERCLE
Vascular connection
ESTABLISHED PARASITE
Emergence
MATURE PARASITE
Flowering
SEEDS
Seed dispersal
Fig. 4.1. Life cycle of a weedy root parasite.
and a haustorium is formed. Intrusive cells of the haustorium penetrate

the host root, ultimately forming a bridge between the vascular systems
of host and parasite. Subsequently, the parasite develops a young plant
(Striga) or a tubercle (Orobanche) that grows underground on the host
root surface for several weeks or months. In some species, lateral adven-
titious roots that emerge from the young parasite can also develop haus-
toria whenever a host root develops nearby. Thus, a single parasite can
have many haustoria, connecting it to roots of one or more hosts. At
maturity, the parasite develops a flowering shoot(s) that emerges above
soil near host plants and sets seeds.
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A. Seed Dormancy and After-Ripening

When the seeds are released from the mature dry fruit they often show
a period of dormancy, during which germination does not occur even
under optimal conditions. This period is supposed to include some
metabolic activities that complete seed preparation for later germination,
and is known as “after-ripening.” In certain Striga species this period
lasts several months, while in certain populations of Orobanche this
period is limited to a few weeks (Ejeta and Butler 1993; Joel et al. 1995b).
After-ripening is influenced by temperature, and seems to limit the ger-
mination of freshly shed seed in the field at the end of a growing sea-
son, ensuring germination only in the next season when host plants are
young enough to support the whole life cycle of the parasite.
B. Wet Dormancy
Even after being imbibed and environmentally primed for germination,
Striga and Orobanche seeds can reenter a low energy dormant state,
reversible with desiccation, if no suitable host is found nearby within a
few days (Mohamed et al. 1998). This secondary or “wet” dormancy
helps to assure seed longevity, which for both Striga and Orobanche can
be over decades (Bebawi et al. 1984; Kebreab and Murdoch 1999; Parker
and Riches 1993).
Whereas primary dormancy coincides with the dry season directly
after maturity, the endogenously induced secondary dormancy seems to
coincide with the subsequent dry seasons (Gbèhounou et al. 1992). It was
also speculated that the relatively short period at which seeds are
responsive to stimulants ensures that the seeds will not germinate too
late in the season, when, despite the presence of a host, the conditions
will not allow completion of the life cycle of the parasite (Matusova et
al. 2004).
C. Germination
A chemical stimulus is needed in order to trigger the germination of root
parasites (Press and Graves 1995). However, some preparatory metabolic
processes take place before the seed can react to stimuli and germinate.
1. Conditioning. Following seed imbibition a moist environment is

required for several days, together with suitable temperatures, in order
to render the imbibed seed responsive to stimulants (Joel et al. 1995b).
This preparatory phase is known as “conditioning,” a complex metabolic
04_4696.qxd 10/25/06 2:20 PM Page 281
and developmental process that consists of a series of events, each cru-

cial in itself, for achieving germination. Then the seeds enter some kind
of stand-by state in which they can persist for relatively long periods
while maintaining their responsiveness to stimulants.
The rate of respiration dramatically changes during conditioning (Bar
Nun and Mayer 1993) indicating that very active metabolic changes are
necessary for the preparation of the seeds for germination. Part of the
oxygen uptake during preconditioning is mediated through the cyanide
resistant alternative oxidase (AOX) pathway. Treatment of the seeds
with inhibitors of AOX during conditioning significantly inhibited their
subsequent germination and reduced the infection of tomato plants by
O. aegyptiaca, indicating that the operation of AOX during condition-
ing has a significant function on the subsequent germination and path-
ogenicity of the root parasite (Bar-Nun et al. 2003).
Fluridone and norflurazon, inhibitors of carotenoid-biosynthesis, pro-
mote the conditioning of Orobanche and Striga seeds (Song et al. 2005;
Chae et al. 2005; Kusumoto et al. 2006), while uniconazole and paclobu-
trazole, inhibitors of the biosynthesis or gibberelin, inhibit seed condi-
tioning and can thus prevent germination (Joel et al. 1989; Zehhar et al.
2002).
A recent molecular study showed that RNA coding for ACC oxidase,
an enzyme in the ethylene biosynthetic pathway, increases during con-
ditioning of S. hermonthica seed (Sugimoto et al. 2005).
2. Germination Stimulation. Parasitic plants of the Orobanchaceae

developed the ability to perceive the presence of adjacent living host
roots by sensing the strigolactones that are released by plant roots, pre-
sumably as signals for their symbiosis with arbuscular mycorrhizal fungi
(Akiyama et al. 2005). These sesquiterpene lactones are active in
extremely low concentrations, from 10–7 to 10–15M (Joel 2000).
Several strigolactones were found in the root exudates of various plant
species (Yasuda et al. 2003) and proved to stimulate the germination of
both Orobanche and Striga. Strigol, which was first identified in the root
exudates of cotton (Gossypium hirsutum L.), was also found in the root
exudates of a variety of other plants (Yoneyama et al. 2004, Sato et al.
2005). Sorgolactone was identified in the root exudates of sorghum and
has high germination stimulant activity on Striga (Hauck et al. 1992;
Awad et al. 2006). Alectrol and orobanchol appear to be the germination
stimulants in the red clover-Orobanche minor association (Yokota et al.
1998), while other strigolactones, strigol and sorgolactone, have also
been identified in red clover (Trifolium pratense L.) root exudates (Sato
et al. 2003). These and similar compounds were later also found in the
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root exudates of other host plants of both Orobanche and Striga (K.
Yoneyama, person. commun.).
Striga seems to have exploited the abundant phytotoxins produced by
sorghum roots as additional germination cues. The hydroquinone SXSg
(sorghum xenognosin for Striga germination), for instance, which has a
biosynthetic origin distinct from the strigolactones, will also stimulate
Striga germination (Boone et al. 1995). SXSg is the reduced form of sor-
goleone, a plant growth inhibitor produced by sorghum roots (Czarnota
et al. 2003; Hejl and Koster 2004).
Yoneyama and coworkers were able to detect and quantify various
strigolactones in root exudates by using tandem mass spectroscopy (Sato
et al. 2003). This method may be an important tool when breeding plants
in which the formation and release of germination stimulants is manip-
ulated (Bouwmeester et al. 2003). There is new evidence based on
mutant and inhibitor studies that the strigolactones are derived from the
carotenoid biosynthetic pathway (Matusova et al. 2005).
So far, only orobanchol produced by red clover, and strigol and stri-
gyl acetate from cotton have been quantified. In both cases, young and
actively growing roots were found to be the major source of germination
stimulants (Sato et al. 2004; Awad et al. 2006).
Distributions of germination stimulation activity after reverse-phase
HPLC analysis of ethyl acetate extracts of root exudates indicate that
there are several strigolactones whose structures are yet to be eluci-
dated. For example, sorghum was found to produce a novel strigol iso-
mer as well as sorgolactone and strigol, and tomato roots release at least
four novel strigolactones, one dehydro- and three tetradehydro-strigol
isomers (Yoneyama et al. 2004).
The capacity of sesquiterpene lactones, which share some structural
features with the strigolactones, to induce germination has been reported
by Fischer et al. (1989). The most active germination stimulation for
Orobanche cumana in the root exudates of sunflower was identified by
Steffens and coworkers as dehydrocostus lactone, a guaiane skeletal
sesquiterpene lactone (Joel et al. 1997a). The structure of this stimulant
is partly similar to portions of the active strigolactones. Dehydrocostus
lactone induces only scanty germination percentages with other
Orobanche species. The relative immunity of tomato and similar plants
to O. cumana attack is solely attributed to their inability to stimulate its
germination. Sunflower is known to contain large amounts of a variety
of sesquiterpene lactones. Recently, Macías and coworkers (Perez de
Luque et al. 2000; Galindo et al. 2002) demonstrated that several other
sesquiterpene lactones also induced the germination of O. cumana, but
not of O. crenata and O. ramosa.
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Additional unrelated compounds that may or may not be present in

host root exudates are capable of inducing germination of Striga, but gen-
erally at concentration magnitudes higher than strigolactones. These
include cytokinins, jasmonates, certain amino acids, and polyols
(Galindo et al. 2004). Ethylene may be the internal switch for the events
leading to Striga germination since exposure to sorghum root exudates
or strigolactones stimulates ethylene biosynthesis in Striga seeds
(Babiker et al. 1993; Logan and Stewart 1991; Jackson and Parker 1991).
ACC synthase (an enzyme involved in ethylene biosynthesis) mRNA lev-
els increased in S. hermonthica seeds after exposure to the germination
stimulant GR24, a synthetic strigolactone. Inhibitors of ethylene biosyn-
thesis blocked the germination stimulant activity of GR24 (Sugimoto et
al. 2005). Applied ethylene can induce Striga spp. germination (Wor-
sham 1987), but Orobanche spp. are generally unresponsive to exoge-
nous ethylene (Galindo et al. 2004).
After germination, the independent life phase of the obligate root par-
asites is characterized by an elongating radicle that may reach a length
of a few millimeters. There is limited evidence that the radicle growth
is guided by chemotropic influence of the potential host root (Williams
1961), presumably through the gradient of exuded germination stimu-
lant (Dubé and Olivier 2001).
D. Haustorial Initiation
In order to attach to their hosts, the obligate root parasites must form a
special organ called the haustorium (from the Latin haurire, to drink).
The term haustorium is used in this review in its broadest sense to
include all its functions from first appearance at induction through
attachment and penetration of host root and acquisition and processing
of host-derived vital substances throughout the life of the parasite.
With initiation of the haustorium, the apical meristem of the radicle
switches from cell divisions in a longitudinal direction to radial divi-
sions resulting in a swelling and proliferation of hair-like projections.
The haustoria of Striga are generally more pronounced in these charac-
teristics than those of Orobanche. As with germination, the parasite
uses host-derived signals to trigger this developmental transition. It is
particularly important that this transition occurs very near the host root
since further radicle elongation stops with haustorial formation. Remain-
ing seed reserves are rapidly consumed once newly germinated Striga
are exposed to haustorial initiation factors (Chang and Lynn 1987).
The chemistry of haustorial induction is distinct from germination
stimulation. Kinetin, simple phenolic compounds, and quinones like
04_4696.qxd 10/25/06 2:20 PM Page 284

2,6-dimethoxy-1,4-benzoquinone (DMBQ) are active haustorial initiators

(Riopel and Timko 1995). There may also be additional tactile signals
involved in haustorial initiation (Wolf and Timko 1991). Preference for
particular compounds in potential host root exudates as recognition
signals for haustorial initiation may vary between parasite species and
strains within a particular species. Genetic variation in recognition of
DMBQ as a haustorial initiation factor was demonstrated among Tri-
physaria spp. and this responsiveness to DMBQ is heritable and influ-
enced by maternal factors (Jamison and Yoder 2001).
Haustorial induction in Striga asiatica with DMBQ has been studied
extensively. Hydrogen peroxide was found at the root meristem during
haustorial initiation of S. asiatica (Kim et al. 1998). The peroxidases use
the H2O2 to oxidize the phenolic components of host cell walls into haus-
torial inducing quinones such as DMBQ. DMBQ then binds to a recep-
tor site on Striga and acts as part of a redox response circuit that
ultimately triggers the formation of the haustorium (Keyes et al. 2000,
2001). Further, it was recently shown that localized auxin and ethylene
accumulate during early development of the attachment organ in T. ver-
sicolor (Tomilov et al. 2005).
E. Attachment and Penetration

Striga asiatica and Agalinis purpurea (L.) Pennell are typical of many
root parasites in that the haustorium that develops on the radicle is cov-
ered with hair-like projections. Upon microscopic investigation, these
haustorial hairs have rough papillate surfaces that secrete a hemicellu-
lose-based adhesive that fixes the parasite to the host root (Baird and
Riopel 1983). A similar adhesive secretion was observed in Orobanche
attachments (Joel and Losner-Goshen 1994). Attachment is apparently
not specific, since S. asiatica will attach to host or nonhost roots (Hood
et al. 1997), and A. purpurea will attach to other plant parts, and even
wood, glass, and plastic (Baird and Riopel 1983). Newly induced haus-
toria can attach to a host root in as few as six hours after induction, but
their ability to attach is lost if they have not contacted a host root within
72 hr (Baird and Riopel 1983). Attachment competency is associated
with the sticky coating of the haustorial hairs that may require chemi-
cal or tactile signals from the host root to maintain (Riopel and Timko
1995).
Penetration of the root to tap host nutrients must occur rapidly since
seed reserves are waning after germination and differentiation of the
preattachment haustorium. During postattachment haustorial develop-
04_4696.qxd 10/25/06 2:20 PM Page 285
ment, the remaining seed storage lipids are mobilized in S. asiatica

(Menetrez et al. 1988).
The penetration mechanism of the various parasites may differ in cor-
relation with the anatomical characteristics of host roots. While most
Striga species attack cereals, the Orobanche species attack dicotyledo-
nous plants, therefore their penetration mechanisms will be discussed
separately.
The intrusive cells of Orobanche push their way between host cells
(Dörr and Kollmann 1974). This is facilitated by enzymatic activities that
change the chemical composition and physical properties of host cell
walls and middle lamella in the path of the haustorium. Pectin
methylesterase (PME) and polygalacturonase activity are released by
young seedlings and infective calli of Orobanche, suggesting their pos-
sible role in penetration (Ben-Hod et al. 1993). Using immunocyto-
chemistry Losner-Goshen et al. (1998) provided direct evidence of the
presence and activity of PME in the host/parasite interface. The enzyme
was found in the cell wall and the cytoplasm of intrusive cells, and in
host cell walls adjacent to parasite cells. A decrease in the degree of
methylation of wall pectins in these host cell walls was also found,
which correspond to PME activity (Losner-Goshen et al. 1998). Whereas
haustorial penetration through host root cortex may be explained by the
activity of pectin degrading enzymes, these enzymes do not seem to be
sufficient for penetration through the root endodermis that includes
cutinized Casparian strips in all radial cell walls. Preliminary immuno-
cytochemical electron microscopy provided first evidence for a possi-
ble Orobanche cutinase activity at the site of haustorial intrusion
through the endodermis (Joel et al. 1998c). After the establishment of the
first direct connection between host and parasite, the procambium in the
young haustorium aligns with host cambium, resulting in the formation
of continuous xylem that bridges the two plants (Joel 2000). It is there-
fore assumed that the mature parasite coordinates its further develop-
ment with that of the host root. In addition to the apoplastic xylem
connections, Orobanche also develops direct symplastic sieve pore con-
nections with the phloem of its host (Dörr and Kollmann 1995).
Striga asiatica parasitizes the roots of cereal plants. Typically, it takes
about 6 days after contacting a sorghum root to reach the vascular core
(Hood et al. 1997). Penetration through the cortex seems to be aided by
enzymatic activity that breaks down wall components of the host corti-
cal cells (Rogers and Nelson 1962). Upon reaching the formidable bar-
rier of the endodermis, the invading cells may proliferate in rows (Rogers
and Nelson 1962). Penetration of the sorghum endodermis is typically
04_4696.qxd 10/25/06 2:20 PM Page 286

delayed for 3 to 4 days in S. asiatica, during which further subcellular

changes occur in the invading haustorium (Hood et al. 1997). With
breaching of the endodermis, intrusions into host vascular elements
occur. In the hemiparasitic Striga, these intrusions occur mainly in
larger host xylem elements (Dörr 1997). After penetrating the xylem
vessels, the invading haustorial cells lose their protoplasts and undergo
wall changes that transform them into water conducting elements con-
tinuous with host xylem (Dörr 1997). No direct connection with host
phloem has been observed in Striga (Rogers and Nelson 1962, Dörr
1997, Neumann et al. 1999).
The interface between haustoria and the invaded host roots of Buch-
nera hispida, Rhamphicarpa fistulosa, and S. hermonthica was studied
under the light and the electron microscope with monoclonal antibod-
ies against pectin, hydroxyproline-rich glycoprotein, and histochemical
staining for lignins (Neumann et al. 1999). This study indicated that the
margin of the contact area between parasite papillae and the host root
surface is sealed with pectins. The lateral interface is characterized by
the presence of compressed, necrotic host cells, whereas the central
interface (contact area between host stele and parasite cells) is generally
devoid of host cell remnants. Phenolic substances and/or lignins were
found at the site of penetration of the haustorium into the host root.
These observations and the accumulation of hydroxyproline-rich gly-
coprotein at the host side of the interface support the view of, at least,
a partial defense reaction in the invaded host root tissues. Within haus-
toria, hydroxyproline-rich glycoproteins were restricted to differentiat-
ing xylem elements, implying a spatio-temporal regulation of these
glycoproteins in developmental processes (Neumann et al. 1999).
Attachment appears to be a prerequisite of the transition to the pene-
tration phase of haustorial development that may involve additional
chemical or tactile signals from the host root. No attempts to chemically
induce cellular changes associated with the penetration phase succeeded
in unattached haustoria (Riopel and Timko 1995). S. asiatica was able to
penetrate the epidermis and at least part of the cortex of several nonhost
roots, suggesting that at its earliest stages, the penetration phase is trig-
gered by factors not unique to suitable host plants (Hood et al. 1997).
However, sustained cellular development that allows intrusion to the
point of vascular connection, may depend on host-supplied factors.
F. Further Haustorial Development

The haustorium continues to mature upon successful establishment of
vascular connections. Externally, a swelling called the tubercle devel-
ops outside the host root by parasites having successfully established
04_4696.qxd 10/25/06 2:20 PM Page 287
vascular connections with their host. The tubercle of Striga hermonth-

ica on maize shows internal lobed structures called the hyaline body,
which is composed of organelle-rich cells and extracellular deposits, and
a vascular core. The endophyte is the part of the haustorium inside the
host root (Gurney et al. 2003). Development of xylem elements in the
vascular core only occurs after penetration, implying that an additional
host derived signal is necessary for triggering this transition (Yoder
1997).
The haustorium that originated from the apical meristem of the radi-
cle is called the “primary haustorium.” This primary haustorium func-
tions throughout the life of the parasite. Adventitious roots form at the
stem base of growing Striga plants and on Orobanche tubercles, from lat-
eral positions on these, and then secondary haustoria may develop pro-
viding additional connections with roots of the primary host or with
roots of neighbouring plants, not necessarily of the same species. Hun-
dreds of secondary haustoria may develop by an individual parasite by
maturity, as with S. hermonthica, O. aegyptiaca, and O. crenata, but they
may be much less prevalent in some Orobanche species, like O. cumana.
In principle, the secondary haustoria are similar in form and function
to primary haustoria (Gurney et al. 2003).
G. Host–Parasite Interaction
After the establishment of vascular connections, the parasite can obtain
the factors it needs for continued growth and development from its host.
Orobanche spp. and S. gesnerioides lack photosynthetic capacity and are
therefore classified as holoparasites (dePamphilis and Palmer 1990,
Bungard 2004). Most Striga spp. are classified as hemiparasites because
upon emergence, they are capable of photosynthesis, but even with car-
bon-fixing capabilities, much of the Striga life cycle is spent under-
ground where photosynthesis cannot occur. Albino Striga plants can
reach maturity (Parker and Riches 1993) as can Striga plants kept in
darkness (Rogers and Nelson 1962. This shows that Striga can obtain all
its carbon building blocks from its host. Growth and photosynthesis
measurements of S. hermonthica on cereal hosts suggest that the para-
site cannot sustain growth without host-supplied carbon (Graves et al.
1990). Stable isotope experiments showed that Striga hermonthica
draws 100% of its carbon from a maize host before and up to 59% after
emergence (Aflakpui et al. 2005). The kinetics of carbon flux during
development of S. hermonthica was quantified (Pageau et al. 1998).
There are some indications that Orobanche may be able to stimulate
dry weight production of its host, especially in the early stages of the par-
asite development (terBorg and Van Ast 1991). This is consistent with
04_4696.qxd 10/25/06 2:20 PM Page 288

the findings that net carbon fixation is higher in tobacco infected by O.

cernua (Hibberd et al. 1999).
However, in the majority of cases, the parasitic weeds significantly
reduce the growth potential of their hosts in agricultural fields, and in
some cases, the photosynthetic activity of the host was also found to be
reduced (Gurney et al. 1995). Moreover, Striga exerts a potent phytotoxic
effect on its host (Ransom et al. 1996) by inducing enzyme and plant hor-
mone changes, disrupting host water relations, and reducing carbon fix-
ation below that expected purely by competition for water, nutrients,
and light (Gurney et al. 1995; Stewart and Press 1990).
Although root parasitic plants are in contact with the soil, it appears
that they take advantage of the organic forms of nitrogen already reduced
by their hosts (Press 1995). Orobanche has phloem connections with its
host (Dörr and Kollmann 1995). On the other hand, established Striga
plants seem not to have any direct phloem connections with their hosts
(Dörr 1997) and so must obtain supplemental carbon needs from the host
xylem sap or through other apoplastic pathways (Press and Whittaker
1993). From 15N studies it appears that a maize host supplies 59% of the
nitrogen used by preemerged S. hermonthica and up to 100% after
emergence (Aflakpui et al. 2005).
The root parasites withdraw nutrients from the host roots via their
haustoria, which form close contacts with host vascular tissue (Kuijt
1969). In spite of the existence of direct links between xylem elements
of the host and parasite (Dörr and Kollman 1995), the supply of solutes
via the xylem to the parasite is likely to be low, because the low rate of
parasite transpiration (Seel et al. 1992) provides only a small driving
force for solute flux between the two organisms, e.g. in Orobanche (Hib-
berd et al. 1999). The interspecific plasmodesmata connecting the host
phloem with that of the parasite in Orobanche (Dörr 1996) indicate that
nutrients may be derived directly from the host phloem. However, we
do not know so far how assimilates are translocated from the host and
through which route.
The greater proportion of carbon moving from host shoot to host root,
and the diversion of assimilate from the host root to the parasite, are usu-
ally attributed to the presence of a strong sink in the parasite. It is pre-
sumed that mannitol serves as a key osmotic agent, used by parasitic
plants to divert nutrients from the host (Harloff and Wegmann 1993;
Delavault et al. 2002). However, the mechanism(s) by which carbon par-
titioning between host and parasite is controlled, is still not clear. One
model predicts that the greater flux of carbon supplied to the host root
by the shoot is due to both the ability of the parasite to remove host car-
bon from the root and by the increase in carbon fixed by the infected
04_4696.qxd 10/25/06 2:20 PM Page 289
plants (Hibberd et al. 1999). It has also been suggested that the acquisi-
tion of carbon and nitrogen in Striga is aided by maintenance of tran-
spiration rates above and osmotic potentials below those of their hosts
(Press and Whittaker 1993; Press 1995).
Nonetheless, the differences in composition between host and para-
site xylem saps indicate that the parasite selectively acquires solutes
from the host. Hibberd et al. (1999) have calculated that the extent of
xylem development at the haustorial connection between Orobanche
and its host is not sufficient to allow the massive supply of the carbon
by a passive movement via xylem connections. They have concluded
that phloem should be the key channel for this purpose.
Since the phloem channels between host and parasite are also limited,
we may expect that active rather than passive transport is responsible
for carbon partitioning in favor of the parasite. Therefore, and unlike the
common opinion that source-sink relations solely provide the driving
force for water and solute translocation between host and parasite, one
should also examine the possibility that the haustorium does not merely
serve as a passive channel through which the sink forces are playing
their role. Instead, it may serve as a mediating element that actively
pumps its nutritional needs from the host (Joel et al. 1998c).
The “hyaline body,” which lies in the central zone of the haustorium
of some hemiparasites of the Orobanchacea, and which considerably
enlarges throughout the development of the parasite, may have a key role
in this putative active transport. While phloem and xylem usually go
side by side along the plant axis, in the haustorium the hyaline body
develops between them, encapsulating the ramifying xylem while also
lying adjacent to the phloem. The dense cytoplasm with abundant endo-
plasmic reticulum and dictyosomes, and the large nuclei (Visser et al.
1984), which are characteristic of the cells of the hyaline body, resem-
ble the structure of glandular cells that are active in short distance trans-
port in plants. This typical ultrastructure may indicate that the hyaline
body is highly active metabolically, which may in turn link it to possi-
ble involvement in active translocation of metabolites from the con-
ductive tissues of the host to the parasite.
It was observed that haustoria accumulated a large amount of nitrate,
and it was hypothesized that this might reflect the function of this com-
pound mainly as a major osmotically active solute in the haustoria
(Pageau et al. 2003). Striga hermonthica can reduce host-derived nitrate,
especially in shoots (Igbinnosa and Thalouarn 1996). Pageau et al. (2003)
hypothesized that concurrent aspargine synthetase and glutamate syn-
thase (GOGAT) activities may explain the high enrichment of gluta-
mine in the roots of this parasite. There were also indications of rapid
04_4696.qxd 10/25/06 2:20 PM Page 290

turnover of aspargine in the haustoria. By contrast, they found an inten-

sive nitrogen flux toward aspargine in the shoots of S. hermonthica,
which apparently results from the direct aspargine transfer from the host,
complemented by an aspargine synthesis from the host-derived nitrate.
On the other hand, while the glutamine concentration in xylem sap was
higher than that of aspargine, the glutamine pool was very small in the
shoots of the parasite. This strongly implies a rapid utilization in the
shoots of the glutamine arriving in the transpiration stream, essentially
for aspargine production. Delavault et al. (1998) isolated a cDNA from
the facultative root-hemiparasite Triphysaria versicolor (Oroban-
chaceae), showing significant homology with aspargine synthetase, and
suggested a putative role for aspargine synthetase in nitrogen uptake
from the host.
H. Seed Production and Dispersal

Scale leaf pairs continue to initiate along the growing stem of Striga, and
within six weeks the young shoots emerge above ground (Stewart 1987).
Flowering occurs within six weeks of emergence and is day neutral
(Stewart 1987). Flowering of Orobanche spp., which may take about two
weeks following emergence, is likewise unaffected by day length (Parker
and Riches 1993). Light is, however, the stimulus that initiates flower
development on the Orobanche stem. Therefore, we may also find flow-
ering stems inside deeply cracked soil.
Some Striga and Orobanche species are self-pollinating while others
are outcrossers (Musselman et al. 1981). However, some species of the
Orobanchaceae also have the ability to form seeds without fertilization
(Pazy 1998; Plitman 2002). Orobanche aegyptiaca, which is known as
an outcrosser and is often pollinated by insects, providing both pollen
and nectar as a reward, will self-pollinate if not visited by insects. This
is facilitated by the elongation of the stamens to a position that allows
pollen to be released on the receptive stigma (D. M. Joel, unpubl.).
The parasites complete their life cycle within 7 to 16 weeks and their
fruits (capsules) contain mature seeds already two weeks after pollina-
tion (Stewart 1987), depending on host phenology. In fact, the parasites
usually germinate during early stages of host development, and produce
fruits at host maturity. The number of seeds produced by a healthy
Striga hermonthica or O. aegyptiaca plant can exceed 200,000 and in
exceptionally successful parasites may reach half a million (Joel et al.
1995b). Large quantities of long-lived seeds assure the parasite genetic
adaptability to changes in host resistance and cultural practices.
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The minute seeds may easily be transferred from one field to another
by cultivation, and also by water, wind, animals, and especially by vehi-
cles and farming machines. Orobanche seed may remain viable in soil
for decades, and thus exert their damage after 30 or even 40 years. Har-
vesting parasite shoots in forage crops may also assist in spreading the
seeds if used to feed animals, because their manure may then be conta-
minated with parasite seeds, which remain viable after passing through
the alimentary system of animals (Jacobsohn et al. 1987).
I. Host Resistance
Breeding approaches that promise improved efficiency for developing
crop cultivars with resistance to parasitic weeds and designed to take
advantage of the ever-growing knowledge of parasite biology have been
suggested for both Striga (Ejeta and Butler 1993) and Orobanche (Joel
2000). From the previous sections on parasite biology, it is evident that
the overall expression of resistance to the root parasites can be broken
down to specific points in the establishment of the parasitic association.
Where a potential resistance character is expressed, it can be narrowed
to a specific point in the parasitic life cycle rather than just its final effect
on the parasite emergence or on the eventual crop damage. A key to this
approach is the ability to observe the host-parasite association at its ear-
liest stages. This necessitates the use of laboratory techniques. Although
operating under the disadvantage of a largely artificial root environ-
ment, fine phenotyping of resistance (reaction of host plants to attack)
is much more possible in the laboratory than in the field.
Based on the knowledge of host-parasite interactions, it is evident that
resistance in host plants can be dissected into simpler components.
Selection for resistance can be readily directed if genetic variation in
host plants exists in situ or can be created through mutagenesis. The first
opportunity for intervention in isolating variants with host-plant resis-
tance is at the level of parasite germination. Crop genotypes may lack the
ability to stimulate germination of conditioned seeds. Alternatively,
some level of inhibition of seed germination may also prevent para-
sitism. A potential host plant may similarly lack the capacity to stimu-
late haustorial initiation of germinated parasite, or exude compounds
that inhibit the formation of this uniquely parasitic organ. Allelopathic
compounds may be produced by host roots that kill young parasites
before they have the opportunity to attach or they may avoid to some
extent the attachment of parasites through reduced root branching in
the upper soil profile where weed seed inoculum is particularly high.
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Haustorial penetration of attached parasites could be hindered if host

recognition factors are altered to the extent that they prevent triggering
a transition of attachment cells to a penetration mode. Alternatively, if
factors in host roots are required to sustain the energy-intensive cellu-
lar activity of haustorial development during the several days between
attachment and establishment of vascular connections, then a resistant
host root can be imagined that may lack certain preferred metabolites
that are available to the young endophytic tissues of the parasite.
Mechanical barriers to parasitic invasion, perhaps induced by the
attempted penetration, might prevent access to the host vasculature.
Another opportunity for the host to block penetration is recognition of
the invasion as a threat and mobilization of defense responses such as
a hypersensitive response, whereby host tissues surrounding the endo-
phyte may become necrotic.
Even if penetration to the host vasculature is accomplished, certain
incompatible responses may prevent a parasite from thriving or surviv-
ing to maturity. Since there is some degree of vascular continuity
between host and parasite, the compounds present in the host’s sap
will influence the growth and development of the parasite. Host sap may
lack certain preferred metabolites so that the parasite has difficulty
assimilating carbon and nitrogen in the forms needed for optimal
growth. Alternatively, the host may produce osmotic solutes that change
the water potential gradient at the host-parasite interface so that translo-
cation of water and nutrients into the parasite is less favored. The bal-
ance of plant growth regulators in the host sap may also affect the
parasite’s growth and development. A resistant host may be less sus-
ceptible to perturbations in plant growth regulators that parasites are
able to effect in a susceptible host. In this case, the growth of the host
plant would not be influenced in ways that benefit the parasite (e.g., root-
to-shoot balance maintained at normal levels). Alternatively, the host
may produce a mixture of plant growth regulators that, if translocated
into the haustorium, are unfavorable to parasitic growth and develop-
ment. Finally, a resistant host may produce toxic compounds in its sap
that are taken up by the parasite, reducing its vigor or even killing it.
Each of the conceived barriers to parasitic establishment should be
identified in the laboratory and some may even be characterized to the
extent that screening protocols useful for breeding populations could be
developed. Most laboratory efforts would initially be used to identify
new sources of resistant germplasm. Potential sources of resistance act-
ing at different points in the life cycle could then be intercrossed to gen-
erate new populations that can be selected for both desirable agronomic
traits and resistances under improved field methods. Even though most
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field selection efforts have been slow and difficult, some studies reported
positive results with an array of changes made around the experimen-
tal layout, by including choices on uniformity of inoculation, appropri-
ate experimental design, large numbers of replications, resistant and
susceptible checks, adjacent infested and uninfested plots, as well as fur-
ther manipulation of data collected in developing specific indices
(Haussmann et al. 2000b).
Breeding efforts could also be greatly aided by molecular markers
associated with each of the phenotypes contributing to specific resis-
tance reactions. Fine phenotyping in the laboratory can be combined
with detailed genotyping using molecular markers. If appropriate map-
ping populations are developed from parents contrasting for individual
contributing phenotypes, closely linked markers can be used to track
resistance loci throughout the selection process. Perhaps not singularly
effective in preventing successful parasitic establishment, individual
loci that contribute to overall resistance can be identified, and these can
be combined in a single genetic background for broad and durable resis-
tance. Molecular markers could aid in determining the contribution of
candidate phenotypes to overall resistance against the parasitic weeds.
1. Contribution of Basic Research. The new approach in breeding for

resistance to obligate root parasites based on a thorough understanding
of the biology of host-parasite interaction, has been effectively applied
to improve resistance to Striga and Orobanche resistance. New sources
of resistance to these pests have been discovered and to varying degrees,
exploited in breeding programs. The best characterized resistance phe-
notype against Striga is low germination stimulant production. Cultivar
differences in sorghum to stimulate Striga germination are well corre-
lated to field resistance (Hess et al. 1992). Low Striga germination stim-
ulant production in sorghum is controlled by recessive alleles at a single
locus, lgs (Vogler et al. 1996). A bioassay for this character has been
exploited in developing Striga-resistant sorghum cultivars (Hess et al.
1992). Maize mutants that are tagged in several root-expressed terpene
synthase genes are currently being studied for alterations in Striga ger-
mination stimulant production, to establish if there is a relation between
the activity of these genes and the formation of germination stimulants
in maize (Bouwmeester et al. 2003).
Beyond low germination stimulant production by host plants, several
other resistant phenotypes are being discovered, and to some degree,
exploited in breeding programs. Coumarins exuded by the roots of
Orobanche-resistant sunflowers result in reduced germination and
browning of radicles of germinated Orobanche cumana (Serghini et al.
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2001). A laboratory method was used to screen wild and cultivated

sorghums for the ability to cause haustorial initiation of germinated S.
asiatica, and wild accessions of sorghum were found that showed
reduced haustorial formation (Rich et al. 2004). Exudation of phytotox-
ins by the host that kill unattached parasites has been reported in sun-
flowers resistant to O. cumana (Serghini et al. 2001). Evidence for
mechanical barriers to penetration has been reported in certain host-
parasite associations by increased lignification (Maiti et al. 1984), depo-
sition of cellulose layers (Olivier et al. 1991a), and encapsulation
(Labrousse et al. 2001). Hypersensitive responses against attaching
parasites have been reported in resistant cowpeas to attached S. gesne-
rioides (Lane et al. 1994b), resistant vetch to attached O. aegyptiaca
(Goldwasser et al. 2000), and in cultivated and wild sorghums to
attached S. asiatica (Mohamed et al. 2003). The release of toxic sub-
stances that kill or hinder development of haustorial cells were noted
in sorghum-Striga associations (Arnaud et al. 1999; Neumann et al.
1999). An incompatible relationship was described with S. hermonth-
ica on sorghum (Grenier et al. 2001) and on Tripsacum dactyloides
(Gurney et al. 2003) a wild relative of maize, whereby growth and devel-
opment of attached parasites was retarded, even though vascular con-
nections were clearly established. S. hermonthica shows delayed
emergence on resistant maize relative to those growing on susceptible
maize (Adetimirin et al. 2000). Incompatible relationships with resistant
hosts have also been reported for O. cumana growing on sunflower
(Labrousse et al. 2001) and O. crenata on a variety of legumes (Pérez-de-
Luque et al. 2005). In addition to having low germination stimulant
activity to Striga, the resistant sorghum SRN39 possesses an apparent
incompatible response to attached Striga that essentially halts parasite
development at an early stage, even if vascular connections are made.
The low germination stimulant trait is independently inherited from the
incompatible response (Grenier et al. 2001). A similar reaction has ear-
lier been described for the Striga-resistant sorghum var. Framida
(Arnaud et al. 1999). In both resistant sorghums, a small proportion of
attached parasites do establish but show diminished growth and delayed
emergence.
As crop-breeding programs adopt use of laboratory procedures, iden-
tify or create appropriate genetic populations, and employ deliberate
selection for resistance to root parasites, host plants with high levels of
resistance to parasitic weeds would likely emerge. It is interesting to note
that in many of the above examples, potential resistance phenotypes are
derived from wild relatives of crop plants. Molecular markers may facil-
itate the transfer of resistance genes into crop cultivars and facilitate
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pyramiding of multiple resistance genes into agronomically desirable

ones. In sorghum, mapping populations have been developed that are
polymorphic for genes associated with low germination stimulant pro-
duction, low haustorial initiation, mechanical barriers, hypersensitive
response, and incompatible response mechanisms of Striga resistance
(Ejeta 2000; Haussmann et al. 2000a; Grenier et al. 2001). Continued
improvements in laboratory and field evaluation methods would likely
continue to drive gains in resistance to parasitic weeds in all crop plants.
2. The Temperature Effect. Temperature may influence synchronization

of host and parasite development. Several researchers studied the indi-
rect effect of temperature on Orobanche parasitism in susceptible crops,
by altering sowing dates. Delayed sowing of broad bean and lentil, from
autumn to winter, reduced the infection levels of O. crenata and O.
aegyptiaca, probably because of unfavorable conditions for Orobanche
development under low winter temperatures (Van Hezewijk 1994; Mesa-
Garcia and Garcia Torres 1986; terBorg et al. 1986; Sauerborn 1989). Sim-
ilarly, early sunflower sowing under cool winter temperatures reduced
O. cumana infection (Castejón-Muñoz 1993).
The sensitivity of susceptible sunflower to O. cumana and O. aegyp-
tiaca is temperature related. High temperatures accelerated parasitism
(Eizenberg et al. 2003a). Orobanche cumana, O. minor, and O. aegypti-
aca parasitism were positively correlated to temperature in the germi-
nation, attachment, and tubercle production stages (Eizenberg at al.
1998, 2003b, 2004a).
In contrast, the sensitivity of resistant crops to Orobanche decreases
with temperature. The resistance reaction of sunflower to infection by
O. cumana and O. aegyptiaca and of carrot to O. crenata and to O.
aegyptiaca was more significant in higher temperatures (Eizenberg et al.
2001c, 2003a, 2003b). Higher temperatures increase the amount of cer-
tain phytotoxic substances in the infected roots of the resistant sunflower
cultivar ‘Ambar’. It was therefore hypothesized that these substances
may inhibit Orobanche development after its establishment in resistant
host roots (Eizenberg et al. 2001a).
Modeling host-parasite interaction is an important tool for predicting
phenological aspects of its development in the field. Using a minirhi-
zotron allowed direct observation of the underground development of
the parasite in the field, which was used for the collection of pheno-
logical data on host parasite relationship in situ (Eizenberg et al. 2005a).
This is now used for the creation of predictive models regarding the rela-
tions between root parasites and their hosts. Parasitism of O. minor in
red clover could be predicted by growing-degree-days under controlled
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conditions (Eizenberg et al. 2004a). This model was validated under field
conditions (Eizenberg et al. 2005b).
J. Race Development
Breeding programs based on only a few dominant genes are in serious
risk of breakdown of resistance. This breakdown of formerly effective
resistances, although not as rapid as experienced with some other
pathogens, is the nightmare of breeders, and forces them to continuously
search for new sources of resistance even in wild relatives of the crop.
A “classical” example is the interaction between sunflower and popu-
lations of O. cumana, in which up to seven races of the parasite have suc-
cessively developed following the introduction of new resistances into
sunflower (Melero-Vara et al. 2000; Fernández-Martínez et al. 2005).
Like most other weeds, the parasitic weeds also exhibit a high
intraspecific variation that is expressed both within and between pop-
ulations. Therefore, whenever the parasitic plant populations are chal-
lenged with new means for their control, they have the genetic resources
to select new strains that are resistant to the new control agent. This may
well lead to the development of new parasitic biotypes, by selection for
virulence, when challenged by the widespread use of highly resistant
cultivars, or by selection to herbicide resistance when herbicides of the
same target site are frequently applied in the field.
The use of molecular markers is suitable for the identification of path-
ogenic groups within parasite populations (Gagne et al. 1998). Román
et al. (2002a) compared O. crenata populations from two distant zones
of the Mediterranean area, using inter simple sequence repeat (ISSR)
markers. The results clearly divided six populations by region, with the
Spanish populations being more similar to each other than the Israeli
populations.
Host preference may vary and should be taken into consideration
when choosing the right crops to be grown in infested fields, and also
in breeding programs that are aimed to supply resistant seeds in a par-
ticular agricultural region. Joel et al. (1998a) have shown an increase in
genetic distance between Orobanche populations that correlates with
geographical distance even within small regions. This genetic distance
may allow variation in host preference. Similarly, genetic variability
within and among populations of S. asiatica from the Republic of Benin
revealed intra and interpopulation variation. The regression of geo-
graphic distance versus genetic distance was significant (R2 = 0.61**).
Interactions of the different populations with susceptible host geno-
types indicated a high degree of host specialization and different degrees
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of virulence, supporting the hypothesis that different populations of

this parasite may well be considered and treated as ecotypes in plant
breeding programs (Botanga et al. 2002).
Geographic variation in host preference is also seen in both A. vogelii
and S. gesnerioides. Certain populations of these species are able to
attack some cowpea cultivars but not others that are susceptible else-
where (Parker and Polniaszek 1990; Riches et al. 1992). Similar to the
O. cumana races in Europe, which are diagnosed with the aid of sun-
flower differentials (Vrânceanu 1980), five strains of S. gesnerioides
have been classified in West and Central Africa on the basis of their abil-
ity to develop on differential cowpea lines (Lane et al. 1994a, 1997).
Although less systematic research has been completed with A. vogelii,
it is clear that there is also variability in the virulence of populations of
this parasite in different areas of Africa (Riches et al. 1992). Therefore,
one should not take for granted that lines selected as resistant in one
country would necessarily be resistant in other countries (Riches 2001).
K. Diagnosis
1. Morphological Species Identification. Orobanche species are herba-
ceous root parasites that develop erect fleshy flowering stems above the
ground, with scales rather than leaves, and without chlorophyll. The
flowers are distinctly two labiate, with two upper lobes and three lower
lobes. Unlike Striga, the ovary of Orobanche is 1-locular, and the fruit
placentation is parietal. The following is a key for field identification of
weedy Orobanche species:
1. Bracteoles present, go to 2
Bracteoles absent, go to 3
2. Corolla up to 22 mm long, filaments and
connective glabrous O. ramosa
Corolla 20 to 35 mm long, connective
(and sometimes filaments) hairy O. aegyptiaca
3. Filaments inserted about the middle of the
corolla tube, go to 4
Filaments inserted in the lower part of the
corolla tube, go to 5
4. Corolla tubular, often bent downward, seeds
longish O. cumana
Corolla upright, constricted above its middle,
seeds pear-shaped O. cernua
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5. Flowers fetid, corolla dark red or purple

Corolla usually white at least toward the
base, go to 6 O. foetida
6. Corolla up to 2 cm long with small lips,
filaments hairy below O. minor
Corolla >2 cm with large divergent lips,
filaments hairy throughout O. crenata
Striga species are herbaceous root parasites that resemble Orobanche,

but may have green or greenish leaves. Unlike Orobanche, the ovary of
Striga is 2-locular, and the fruit placentation is central. The following
is a key for field identification of weedy Striga species:
1 Parasites of cereals, with green leaves, go to 2

Parasites of dicotyledonous crops, leaves
reduced to scales S. gesnerioides
2 Each calyx lobe carries one vein rib, flowers
pink, go to 3
Two vein ribs per calyx lobe, flowers red,
yellow, or white S. asiatica
3 Bracts below each flower up to 1 to 2 mm
wide, corolla up to 1.5 cm long S. aspera
Bracts 2 to 3 mm wide, corolla 1.5 to 2 cm
long S. hermonthica
2. Molecular Identification. Molecular markers may assist diagnosis

purposes on the species and the population level. Diagnosis is particu-
larly needed due to the differences in host preference. Because of the
minuscule seed size, contamination of fields and crop seed lots by par-
asite seeds is difficult to detect by conventional methods. As these seeds
will only germinate and grow in the presence of a susceptible host, the
early identification of the parasite species in the field by soil sampling
is of great importance to farmers. Joel et al. (1996b, 1998b) developed a
rapid and reliable PCR-assay for diagnostic identification of five differ-
ent Orobanche species, consisting of the development of specific
primers based on unique sequences for each of them. They have also
developed a protocol that allows the identification of single tiny seeds
of these parasitic weeds. Seeds of O. minor were later similarly detected
by PCR-assay consisting of the development of primers based on unique
sequences in the internal transcribed spacers (ITS) regions (Rehms and
Osterbauer 2003). Portnoy et al. (1997) extended the protocol, allowing
04_4696.qxd 10/25/06 2:20 PM Page 299
for the identification of soil-borne parasite seeds from soil samples that
are collected in the field. With the development of Real-Time PCR, we
anticipate that a quantitative diagnostic ability will soon be possible
based on the extraction of DNA directly from soil samples. These meth-
ods should serve as important components in precision agriculture that
gradually replaces the traditional agricultural practices in the industrial
countries.
V. MANAGEMENT
A. General Considerations
Few crops can be protected from parasitic weeds by resistances or her-
bicides. With all other crops, the only means to limit the damage caused
by parasitic weeds focus on reducing soil seed bank, preventing seed set,
and inhibiting seed movement from infested to noninfested areas.
So far, the effectiveness of conventional control methods is limited
due to numerous factors, in particular, the complex nature of the para-
sites that reproduce by tiny and long-living seeds, and are difficult to
diagnose until they irreversibly damage the crop. The intimate connec-
tion between host and parasite also hinders efficient control by herbi-
cides. One of the most suitable control options is the development of
resistant crop cultivars (Cubero 1986; Haussmann et al. 2000a,b). Unfor-
tunately, in many crops no sources of resistance were ever found, and
consequently no resistant cultivars could be produced. Altogether the
available control methods have not proved to be as effective, economi-
cal, and applicable as desired (Joel 2000; Goldwasser and Kleifeld 2004).
Although several potential control measures were developed in the past
decades for some crops, any approach applied alone is often only par-
tially effective and sometimes inconsistent, and affected by environ-
mental conditions.
The only way to cope with the weedy root parasites is through an inte-
grated approach employing a variety of measures in a concerted man-
ner starting with containment and sanitation, direct and indirect
measures to prevent the damage caused by the parasites, and finally
eradicating the parasite seedbank in the soil.
Much research is needed in order to develop new means for parasitic
weed control. Basic research should provide new targets for control
within the life cycle of the parasites and among their metabolic activi-
ties. The genomic research of root parasites, which has already started,
is likely to help in an overall understanding of some key aspects of
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parasitism. Some model plants, like Arabidopsis thaliana and Medicago

truncatula have been used for studies on host reaction to infection
(Westwood 2000; Rodríguez-Conde et al. 2004), and the parasite Tri-
physaria versicolor, as a model parasite (Yoder 1997). These plants serve
as valuable sources for genomic understanding of host-parasite interac-
tion. In addition, research also takes advantage of some crop plants, like
sunflower, tomato, and sorghum, which serve as important hosts for key
parasitic weeds, with the advantage that they may allow an immediate
application of any new idea directly in the field.
In the following, we present details of the major approaches for the
control of weedy root parasites. Since there are some basic differences
between the agricultural systems that are infested by Striga and the sys-
tems affected by Orobanche, we have dedicated separate sections for
each of them. Nevertheless, some information on Striga management is
also highly relevant to Orobanche infested systems, and vice versa.
B. Orobanche Management
1. Chemical Control. Chemical control of Orobanche is complicated
because: (1) herbicides had been effective only as a prophylactic treat-
ment, since in most cases the actual infestation level in the field is usu-
ally unknown; (2) seeds continuously germinate throughout the season;
(3) the parasite is directly connected to the host; and (4) the host should
be selective to the herbicide without reducing its phytotoxicity if the her-
bicide is to be applied to the parasite through the host via its conduc-
tive tissues.
There are very few herbicides that are able to selectively control the
parasites (Kleifeld et al. 1998; Goldwasser and Kleifeld 2004; Gressel et
al. 2004). The herbicides that are currently in use for Orobanche control
are glyphosate, inhibitor of 5-enolpyruvylshikimate-3-phosphate (EPSP)
synthase—a key enzyme in the biosynthesis of the aromatic amino acids,
and imidazolinones and sulfonylureas, inhibitors of acetolectate syn-
thase (ALS), key enzyme in the biosynthesis of branched-chain amino
acids. Sulfonylurea herbicides are selective systemic herbicides that
can be absorbed through foliage and roots with a rapid acropetal and
basipetal translocation (Schloss 1995). The imidazolinone herbicides are
translocated by the host to meristematic tissues, in which the enzyme
is highly active. In some cases, depending on the host, imidazolinone
herbicides may leak to the rhizosphere (Shaner and O’Connor 1991).
Herbicides should be applied during the initial stages of the parasite
development, i.e., to seedlings or to small young Orobanche plants that
are attached to host roots. Knowledge of the phenology of Orobanche is
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essential for its effective chemical control. Application must be repeated

in time intervals of 2 to 4 weeks, because Orobanche seeds may germi-
nate throughout the season, and may therefore be reestablished on newly
developed hosts roots. Based on growing-degree-days (GDD), Eizenberg
et al. (2004a, 2005b) recently suggested a model for O. minor develop-
ment and for the suitable timing for a precise chemical control of this
species in red clover (Eizenberg et al. 2006).
Three main chemical control approaches are used in agriculture: (1)
foliar application of herbicides; (2) application of herbicides through the
soil; and (3) herbicide application in combination with the use of trans-
genic crops that possess target-site resistance to the corresponding her-
bicide.
Foliar Application of Herbicides. There are two main concepts for con-
sidering chemical control of Orobanche. Control with systemic herbicides
that are translocated through the host phloem to the attached parasite that
serves as a strong sink. In this case, the Orobanche underground devel-
opmental stages should be monitored because only the young attach-
ments can effectively be controlled. On the other hand, if the herbicide
is applied too early, only the few attachments present on the roots will
be controlled while the new germinating seeds, and attachments formed
after herbicide application, will not be affected by the herbicide.
In general, foliar herbicide application for Orobanche control requires
lower herbicide rates compared to those applied for nonparasitic weed
control. Sequential foliar application of low rates of glyphosate for
Orobanche control is effective on few hosts of the Apiaceae, Brassi-
caceae, and Fabaceae (Jacobsohn and Kelman 1980; Mesa-Garcia and
Garcia-Torres 1985; Sauerborn et al. 1989b). However, glyphosate reduces
host ability to defend itself against pathogens (Sharon et al. 1992). Foliar
application of imazapic for Orobanche control is effective in sunflower,
carrots, parsley, celery, faba bean, and vetch. Imazethapyr is registered
for controlling O. crenata in garden and field pea in Israel. In some
cases, herbicides control the parasite but are only moderately selective
to the host. Imazapic does not inhibit the vegetative growth of sun-
flower, but high rates of the herbicide applied in the bud formation
stage injure and disturb normal sunflower head formation. Foliar appli-
cation of imazapic in potato controls O. ramosa, O. aegyptiaca, and O.
cernua but causes severe tuber deformations. In carrot, Orobanche is
controlled with sequential foliar treatments with imazapic and imaze-
thapyr. Though effective in controlling the parasite, imazethapyr treat-
ments cause heavy damage to carrot roots, characterized by radial and
vertical cracks.
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Application of Herbicides through the Soil. Sulfonylurea herbicides

effectively control imbibed and germinated seeds or young attachments
of Orobanche when applied directly to the soil in tomato and potato
fields (Hershenhorn et al. 1998 a, b; Kleifeld et al. 1998). The control of
young attachments is due to direct contact with the herbicide or through
the host, which may absorb the herbicide by its roots, and allow its
translocation to the parasite (Plakhine et al. 2001). Herbicide delivery to
the soil can be achieved by several means, including chemigation—the
delivery of the herbicide through the irrigated water. This can be accom-
plished with either drip or sprinkler irrigation. Accordingly, the herbi-
cide can be applied preplanting and mechanically incorporated into
soil, or it can be applied postemergence or postplanting and incorpo-
rated into soil by sprinkler irrigation. Chemigation is effective for
Orobanche control in tomato and potato.
Chemigation faces some application problems. For example, large-
scale chlorsulfuron sprinkler chemigation applied under unfavorable
conditions, e.g., under windy weather conditions, may damage the crop
because of uneven herbicide delivery imposing high level of the herbi-
cide on tomato foliage in some spots in the field. Hershenhorn et al.
(1998c) suggested three chemigations of chlorsulfuron for controlling
Orobanche in tomato. Late in the season, Orobanche inflorescences
emerged in the center of the tomato beds near the drip irrigation pipe,
presumably because the irrigated water washed the herbicide from the
rhizosphere. Adding chemigation via the drip irrigation water prevents
the late Orobanche shoot emergence (Hershenhorn et al. 1998c). Due to
the complexity of sprinkler herbicide chemigation, Eizenberg et al.
(2001b), suggested sprinkler chemigation of the herbicide in accordance
with field infestation levels, i.e., to sprinkler irrigate moderately infested
fields only once followed by four sequential drip chemigations. Indeed
chlorsulfuron was highly effective in Orobanche control but the com-
plexity of its delivery and its long residual effect in the soil required the
development of a new approach in order to deliver the herbicide uni-
formly into the soil. The newly developed approach consisted of the
application of the herbicide on tomato foliage and followed by sprinkler
irrigating the field in order to incorporated the herbicide into the soil.
The number of herbicide applications may vary between one and three,
and should depend on the field infestation level. Using this approach
with foliar application of rimsulfuron or sulfosulfuron, Orobanche
aegyptiaca was effectively controlled in tomato (Eizenberg et al. 2003d).
As described above, Orobanche shoot emergence in the center of the bed
at late season requires one more treatment of drip chemigation (Eizen-
berg et al. 2001b, 2003c). Sulfosulfuron was found to be more effective
04_4696.qxd 10/25/06 2:20 PM Page 303
than rimsulfuron in Orobanche control at high infestation levels because

of its longer residual effect. In addition, sulfosulfuron is also highly
effective in controlling some other troublesome weeds such as black
nightshade (Solanum nigrum L.s.l.), pigweed (Chenopodium album L.),
and nutsedge (Cyperus rotundus L.) (Eizenberg et al. 2003e).
Foliar applications of sulfonylurea herbicides on tomato grown in
charcoal topped pots was ineffective in controlling O. aegyptiaca, indi-
cating that the herbicides of this group cannot be translocated to the par-
asite through the conductive system of the host (Eizenberg et al. 2003c,
2004b; Plakhine et al. 2001).
The potential of herbicides to directly control Orobanche seedbank in
soil was tested by Hershenhorn et al. (1998a) and Plakhine et al. (2001).
The sulfonylurea herbicides: bensulfuron, chlorsulfuron, nicosulfuron,
primisulfuron, rimsulfuron, thifensulfuron, triasulfuron, sulfosulfuron,
flazasulfuron, and ethoxysulfuron that were applied directly on pre-
conditioned and germinated Orobanche seeds in petri dishes signifi-
cantly reduced O. aegyptiaca germination (except nicosulfuron) and
radicle elongation (except bensulfuron) of the parasite.
Target Site Herbicide Resistance in Crops. This technique is perhaps one
of the most promising solutions for controlling Orobanche in many
crops. Complete control of O. aegyptiaca without any significant effect
on the crop or its yield was achieved using glyphosate on EPSP syntase
resistant oilseed rape, chlorsulfuron on ALS-resistant tobacco (Joel et al.
1995a), and asulam on tobacco plants with asulam resistance (Surov et
al. 1998). Herbicide resistance can be achieved in crop plants by trans-
formation, mutagenesis, or selection of already existing resistant indi-
viduals.
2. Host Plant Resistance. The development of improved cultivars with

resistance to a single pathogen is often straightforward if a good source
of resistance is available and an efficient, easily controlled and practi-
cal screening procedure exists to provide sufficient selection pressure.
Unfortunately, this is seldom the case with parasitic weeds. Resistance
against most parasitic weeds is difficult to access, scarce, of complex
nature, and of low heritability, making breeding for resistance a difficult
task (Rubiales 2003). In spite of these difficulties, significant success has
been achieved in some crops. In a few instances, Orobanche resistance
of simple inheritance, acting after parasite penetration, has been iden-
tified and widely exploited in breeding. This has been particularly
important allowing a rapid progress in sunflower breeding against O.
cumana (Ish-Shalom-Gordon et al. 1993; Domínguez 1996). However,
04_4696.qxd 10/25/06 2:20 PM Page 304

breeding programs based on only a few dominant genes are in serious

risk of breakdown of resistance. In fact, up to seven races of O. cumana
(named A, B, C, D, E, F and G) attacking sunflower have been identified
(Melero-Vara et al. 2000; Fernández-Martínez et al. 2005). This break-
down of formerly effective resistances, although not as rapid as experi-
enced with some other pathogens, is the nightmare of breeders, and
forces them to continuously search for new sources of resistance even
in wild relatives of the crop. A number of single dominant genes for
resistance named Or1 through Or5 have been progressively identified
and introduced in commercial sunflower hybrids as soon as new O.
cumana races appeared.
Resistant Sunflower. The first sunflower cultivars resistant to O. cumana

were developed in the former USSR between 1912 and 1917. But by 1925
susceptibility of these cultivars to O. cumana races was reported for
Ukraine and Moldova. The Orobanche populations were thus respec-
tively designated as races A and B (Vrânceanu et al. 1980). Intensive
efforts were made to locate resistance to the new races, and this was
found among a landrace collected from a farmer’s field in Ukraine. New
resistant cultivars were released, such as ‘Jdanov 8281’ resistant to race
B, and ‘Peredovick’, resistant to races A and B. In the mid 1960s, a new
race named C, with virulence toward all the resistant cultivars was iden-
tified in Moldava and Ukraine. In 1990, a new race, D, was first identi-
fied in the Krasnodar region. Resistance gene Or5 to race E was identified
in 1989 and incorporated into hybrids (Domínguez et al. 1996). Races A
through E were identified using a set of Romanian and former USSR sun-
flower cultivars as differential series (Vrânceanu et al. 1980): ‘Kruglik A-
41’ (gene Or1 for resistant to race A), ‘Jdanov’ 8281 (Or2 to race B),
‘Record’ (Or3 to race C); S-1358 (Or4 to race D); and P1380 (Or5 to race
E). Nevertheless, the complexity of this pathogen suggests that what is
known as races C, D, E , and so forth, may differ from one country to
another. It implies the need for standardization of the screening method
and identity of the differentials used across countries.
Race F, overcoming all the known resistance genes (Or1,2,3,4,5)
appeared in 1995 in Spain and is spreading rapidly. Resistance has been
found both in cultivated and wild sunflower (Fernández-Martínez et al.
2000; Jan et al. 2002), but a new race (G) that overcomes race F resistant
lines has already been identified (Molinero-Ruiz and Melero-Vara 2005;
Fernández-Martínez et al. 2005). Virulent populations overcoming race
E resistant lines, have also been reported in Romania and Turkey, and
have also been designated as race F. However, it seems that these new
04_4696.qxd 10/25/06 2:20 PM Page 305
races from Spain, Romania, and Turkey have different degrees of viru-
lence (Fernández-Martínez et al. 2005).
Wild Helianthus species constitute the major source of resistance
genes for sunflower breeding, but cultivars are also a valuable source of
resistances to race F of O. cumana (Fernández-Martínez et al. 2000). Four
germplasm populations, BR1 to BR4, resistant to race F have been devel-
oped through interspecific hybridization of cultivated susceptible mate-
rial and the perennial wild resistant species H. divaricatus, H.
maximiliani, and H. grossesserratus Martens (Jan et al. 2002). Several
cycles of disease screening and selection resulted in the development of
four lines, P-96, K-96, R-96, and L-86, uniformly resistant to races B, E,
and F and susceptible or showing segregation to race G, and AM-1, AM-
2, and AM-3 showing quantitative resistance to race F (Fernández-
Martínez et al. 2004).
Resistance of complex inheritance has also been identified in sun-
flower (Pérez-Vich et al. 2004) but was neglected in the past, giving pri-
ority to single gene resistance. However, sunflower breeders are starting
to realize the need to accumulate levels of quantitative resistance
together with qualitative resistance (Pérez-Vich et al. 2004; Fernández-
Martínez et al. 2005). Various resistance mechanisms against O. cumana
have recently been described in wild species of Helianthus (Labrousse
et al. 2001) and these are being transferred into cultivated sunflower.
Only moderate to low levels of incomplete resistance of complex
inheritance against Orobanche has been identified in other crops, such
as in parsley (Goldwasser and Kleifeld 2002), tomato (Qasem and Kas-
rawi 1995), oilseed rape, carrot (Zehhar et al. 2003), legumes (Rubiales
et al. 2006b), and pepper (Piper spp.) (Hershenhorn et al. 1996). This has
made selection more difficult and slowed down the breeding process.
The quantitative resistance resulting from tedious selection procedures
has resulted in the release of cultivars with useful levels of incomplete
resistance combined with a degree of tolerance (Cubero et al. 1994;
Khalil and Erskine 1999).
Resistance in Legumes. Breeding of legume crop cultivars resistant to O.

crenata was initiated with faba bean improvement in the early 1960s
(Elia 1964). Only low levels of resistance to O. crenata was available in
faba bean until the appearance of the Egyptian line F402 (Nassib et al.
1982). Breeding for Orobanche resistance in faba bean is a difficult task,
but significant successes have been achieved (Cubero and Hernández
1991; Cubero and Moreno 1999; Khalil and Erskine 1999). Some acces-
sions with low to moderate levels of resistance and/or tolerance had
04_4696.qxd 10/25/06 2:20 PM Page 306

been reported, such as ‘VF172’, ‘Express’, BPL2210, and ‘Locale di

Castellano’, but the first significant finding of resistance was the selec-
tion of the resistant line F402 (Nassib et al. 1982) that showed a high
level of field resistance as well as agronomically favorable characteris-
tics, and gave origin to ‘Giza 402’ that was widely used in Egypt. The line
W1071 and various other cultivars were selected out of ‘Giza 402’, and
are collectively identified as ‘family 402’.
Resistance against O. foetida has been identified in faba bean
germplasm in Tunisia. Some lines (674/154/85 L3-4 and 402/29/84)
selected against O. crenata have also shown a high level of resistance to
O. foetida, with a high yield potential (Kharrat and Halila 1994). Resis-
tance to O. crenata does not seem to protect against O. foetida infection,
but combining resistance to both species has been possible, by selecting
for O. foetida resistance in O. crenata resistant germplasm.
Little resistance is available within field pea germplasm against O. cre-
nata (Rubiales et al. 2003b), but promising sources of resistance have
been identified in wild relatives within the genus Pisum (Rubiales et al.
2006b), which have successfully been hybridized with cultivated pea
(Rubiales et al. 1999; Pérez-de-Luque et al. 2005a). One such resistance
has been mapped (Valderrama et al. 2004; Fondevilla et al. 2005).
Resistance is also very limited in cultivated grass pea and chickling
vetch (L. cicera L.) but is available in related Lathyrus species (Linke et
al. 1993; Sillero et al. 2006). No resistance has been identified in lentils
(Sauerborn et al. 1987; Khalil and Erskine 1999). However, resistance is
frequent in common vetch and chickpea germplasm and cultivars (Gil
et al. 1987; Rubiales et al. 2003a) as well as in their wild relatives (Linke
et al. 1993; Rubiales et al. 2004, 2006a; Sillero et al. 2006). Resistance to
O. aegyptiaca has been found in Vicia atropurpurea Desf. (Goldwasser
et al. 1997).
Dissecting the escape and resistance factors will help to detect exist-
ing genetic diversity for mechanisms that hamper infection (Jorrín et al.
1999; Labrousse et al. 2001; Rubiales et al. 2003c). Combination of dif-
ferent resistance mechanisms into a single cultivar should provide a
more durable outcome. This can be facilitated by the adoption of marker-
assisted selection techniques, together with the use of in vitro screen-
ing methods that allow dissecting parasitic weed resistance into highly
heritable components (Haussmann et al. 2000b; Román et al. 2002b;
Pérez-Vich et al. 2004).
Resistance Mechanisms. Resistance is a multicomponent event, the

result of a battery of escape factors or resistance mechanisms acting at
different levels of the infection process. Host plants might escape infec-
04_4696.qxd 10/25/06 2:20 PM Page 307
tion by reduced root biomass and by root architecture that avoids the soil
layer in which the seeds of the parasite are more common. The host may
limit damage (tolerance) by factors that influence source-sink relation-
ships, such as osmotic pressure (Wegmann et al. 1991). Although low
induction of germination was considered to play a minor role in resis-
tance to Orobanche (terBorg 1999), this trait has recently been found in
some accessions of a range of legumes, including vetches, peas, chick-
pea, and grass peas (Rubiales et al. 2003b,c; Sillero et al. 2006; Pérez-de-
Luque et al. 2005a) and sunflower (Jorrín et al. 1999; Labrouse et al.
2001).
Necrosis and/or the development of protective layers that block the
development or the intrusion of the haustorium inside host tissues have
been reported in sunflower to O. cumana (Labrouse et al. 2001), carrot
to O. ramosa (Zehhar et al. 2003), Vicia atropurpurea to O. aegyptica
(Goldwasser et al. 1997), and common vetch (Pérez-de-Luque et al. 2001,
2005b), faba bean (Zaitoun et al. 1991), and chickpea to O. crenata
(Rubiales et al. 2003c). The unsuccessful penetration of O. crenata
seedlings into legume roots cannot be attributed to a typical necrosis in
the host. It seems to be associated with lignification of host endodermis
and pericycle cells at the penetration site. The accumulation of secre-
tions at the infection site may lead to the activation of xylem occlusion,
another defense mechanism that may cause further necrosis of estab-
lished tubercles (Pérez-de-Luque et al. 2006a). Protein cross-linking in
the host cell has also been proposed as a mechanism of defence in pea,
halting penetration of the parasite in the host cortex before reaching the
central cylinder, with accumulation of H2O2, peroxidases, and callose in
neighbouring cells (Pérez-de-Luque et al. 2006b).
Germplasm Collections. Variation for resistant traits can be found in

germplasm collections. Landraces have been widely replaced by homo-
geneous cultivars that may not possess the combined tolerance and
resistance already accumulated in landraces or wild accessions by nat-
ural selection. Genetic resources remain highly unexplored and under-
used and might contain additional sources of resistance.
Apart from the conventional field and pot screening methods, further
laboratory assays, which allow the nondestructive, rapid, and inexpen-
sive evaluation of individual plants for resistance, are desirable. The
development of marker-assisted selection (MAS) techniques for broad-
based polygenic resistance is a particularly promising approach since
direct Orobanche resistance tests are difficult, expensive, and some-
times unreliable. Quantitative trait loci (QTLs) for resistance to race E
and F of O. cumana have been identified in sunflower (Pérez-Vich et al.
04_4696.qxd 10/25/06 2:20 PM Page 308

2004). QTLs have also been identified for O. crenata resistance in faba
bean (Román et al. 2002b), and pea (Valderrama et al. 2004; Fondevilla
et al. 2005). The development of markers tightly linked to QTLs previ-
ously detected in a map and the conversion into codominant sequence
characterized amplified regions (SCAR) is the most immediate need.
These markers located near to the resistance QTLs would enable the sat-
uration of relevant genome regions in order to obtain good candidate
markers to be exploited in MAS. Five SCAR markers linked to Or5 gene
conferring resistance to race E have been developed (Lu et al. 2000). In
the near future, new genomic approaches will serve to assist breeders
and geneticists in identifying promising resistant genotypes and will
facilitate the efficient transfer of the resistance genes among breeding
lines. Dissection of the molecular responses to Orobanche has been ini-
tiated. The first defense reaction recorded on the molecular level was the
activation of the basic PR-1 gene promoter following O. aegyptiaca
attachment on transformed tobacco roots (Joel et al. 1996a; Joel and
Portnoy 1998). This induction of a host defense gene by Orobanche sug-
gests that the host at least partially identifies the invader, even though
it may be susceptible to the parasite. It therefore appears that at least part
of the signaling pathway leading to host resistance is activated. Simi-
larly, the tomato hmg2 promoter in transgenic tobacco was expressed as
early as one day after root penetration by O. aegyptiaca (Westwood et
al. 1998). The promoter hmg2 encodes a protein involved in isoprenoid
biosynthesis pathway and is activated specifically during defense
responses associated with phytoalexins and sesquiterpenes production.
Several genes of the jasmonate (lox, aos, aoc, PR-3, and thi2.1) and of
the ethylene (acc2) pathways were later found to be induced by O.
ramosa in Arabidopsis thaliana (L.) Heynh (Vierira Dos Santos et al.
2003a,b). However, genes regulated by salicylic acid (PR-1, PR-2, and PR-
5) and camalexin (asa1 and pai1) were not activated by O. ramosa. A
stronger overall defense response has been detected against O. cumana
in a resistant sunflower line compared with a susceptible one, involv-
ing marker genes of the salicylic acid pathway (Thoiron et al. 2005).
Recent analyses performed on three pathosystems (Arabidopsis or
tomato/O. ramosa; sunflower/O. cumana), showed that hosts respond
to Orobanche by inducing an array of general defense pathways such as
phenylpropanoids, jasmonate and ethylene pathways, cell wall rein-
forcement, PR proteins, and reactive oxygen species induction (Thoiron
et al. 2005).
Proteins that correspond to enzymes of the nitrogen assimilation path-
way (glutamine synthetase) or typical pathogen defense, PR proteins,
including 1,3-glucanase and peroxidases, increased in pea resistant
04_4696.qxd 10/25/06 2:20 PM Page 309
accession after infection by O. crenata (Castillejo et al. 2004; Jorrín et al.

2006). Resistance has been correlated with an increase in the level of
phenolics and peroxidase activity in V. atropurpurea infected by O.
aegyptiaca (Goldwasser et al. 1999), sunflower infected by O. cumana
(Serghini et al. 2001), and also in faba bean, pea, and chickpea infected
by O. crenata (Wegmann et al. 1991; Pérez-de-Luque et al. 2005a).
3. Eliminating the Parasite Seed Bank. The main obstacle in the long-
term management of Orobanche infested fields is the durable seedbank
that may remain viable for decades, and gives rise to only a very low
annual germination percentage, if at all. As long as the seed bank is not
controlled, the need to apply means to control the parasite will persist.
Three main approaches are possible for seedbank demise: fumigation,
solarization, and biological control.
Solarization. Solarization utilizes the sunlight in the summer to produce
high temperatures under clear polyethylene mulch that covers the soil
for several weeks (Katan and Vay 1991). The temperature under the
mulch may reach 55°C. Nevertheless, in order to achieve effective con-
trol, Orobanche seeds should be in the imbibed state, therefore soil
must be wet at the application time (Jacobsohn et al. 1980). Mulching
wet soil with transparent polyethylene sheets for a period of 4 to 8
weeks during the warmest season proved to be effective. The tempera-
tures under the polyethylene sheet are raised by 9° to 12°C at a depth of
5 cm. The lethal effect is caused by the interactions of daily fluctuating
elevated temperature and accumulation of various volatiles within the
soil atmosphere (Jacobsohn et al. 1980). Soil solarization was success-
fully applied in the Middle East for tomato, eggplant, faba beans, lentil,
and carrot (Abu-Irmaileh 1991; Jacobsohn et al. 1980; Sauerborn et al.
1989a). Although soil solarization is effective under optimal conditions
to the upper soil layer (15 to 20 cm), it is expensive and may be applied
only at localized geographical regions with long sunny summers.
Fumigation. This method takes advantage of the toxic effect of various
compounds that act in their gaseous phase and are able to kill Orobanche
seeds.
Fumigation with methyl bromide effectively controls Orobanche seeds
in soil if correctly applied. Soil should be extensively rotary-cultivated
and kept moist for 7 to 14 days before application. Following methyl bro-
mide application, the treated soil is immediately covered with plastic
mulch for 48 hr (Foy et al. 1989). Methyl bromide application is almost
completely banned for use because of its negative environmental effects.
However, methyl bromide may be used to kill parasite seeds in heavily
04_4696.qxd 10/25/06 2:20 PM Page 310

infested soil, when soil rehabilitation is needed. This has been used, for
example, in Australia as part of the Branched Broomrape Eradication
Program (Warren 2005).
Metham sodium is usually applied as a liquid that releases the active
ingredient methyl isothiocyanate. This chemical is toxic to Orobanche
seeds but is only partially effective because it evaporates rapidly from
soil. Metham sodium is highly expensive. Plastic mulching may increase
its efficacy but will also increase costs (Goldwasser et al. 1995).
Dazomet is a solid compound that also releases methyl isothiocyanate
when wetted. The dazomat granules should be incorporated into the
upper 10 to 20 cm soil layer and should be activated by irrigation. The
treatment is effective in controlling Orobanche seeds but is more costly
than metham sodium (Khalaf et al. 1994).
Other fumigants such as ethylene dibromide, methyl iodide, and
telone (1,3-dichloropropene) were tested as possible substitutes for
methyl bromide on an experimental basis or on limited commercial use.
All are much less effective than methyl bromide and are highly costly
(Foy et al. 1989; McDonald, 2002; Goldwasser and Kleifeld 2004). It
should also be noted that all the fumigants are highly toxic to humans
and mammals and therefore, extreme care should be taken while using
them. In most countries, only certified personnel are allowed to apply
these chemicals.
4. Biological Control. Biological control is particularly attractive in sup-

pressing root parasitic weeds in annual crops because of the intimate
physiological relationship of the biocontrol agents with their host plants
and their high specificity. Both insects and fungi that attack parasitic
angiosperms have been isolated. However, because of the enormous
seed production by Orobanche, the ability of the seeds to persist for
decades, the very low annual percentage of seed germination, and the
vast damage caused to the host by unemerged plants, Orobanche can-
not be regarded as an ideal target for biological control, unless the bio-
logical agent predates directly on the seedbank in soil.
Insects. Most of the insects that have been reported to occur on
Orobanche species are polyphagous without any host specificity and
thus, damage to these parasitic weeds is limited (Klein and Kroschel
2002). However, for biological control only oligo- and mono-phagous
herbivorous insects are of interest. The fly Phytomyza orobanchia Kalt.
(Diptera: Agromyzidae) is one of the few insects that are reported to be
host-specific, only attacking Orobanche species. The distribution of this
fly coincides with the natural occurrence of Orobanche spp. This insect
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prevents seed production through the development of larvae inside the

seed capsules of its target host and thus reduces their reproductive
capacity and seed dispersal. However, the effectiveness of preventing
seed set may contribute only in decreasing replenishment of the seed-
bank with freshly developed seeds, but may not be sufficient to directly
decrease the soil seed bank (Smith et al. 1993; Klein et al. 1999).
A factor that may limit the effect of natural populations of P.
orobanchia is soil cultivation, especially deep ploughing, by which
hibernating pupa can be destroyed and/or buried. Further limiting fac-
tors of cultivation are pesticide applications against crop pests if these
coincide with the flight periods of the beneficial insect. Moreover, P.
orobanchia suffers from indigenous antagonists that may have an impor-
tant impact on its population level.
The massive propagation and innundative release of this insect in
infested areas should, however, bypass these limitations, and have the
advantage of reaching single emerging Orobanche plants and prevent-
ing them from massive seed production.
Fungi. The virulence of parasitic weeds, their regional occurrence, and
their parasitic lifestyle make them suitable targets for biocontrol by bio-
herbicidal approach—multiplication and periodic release of indigenous
microbial agents for sustained control of the target species. Periodic
releases will be necessary because biotic and abiotic factors limit their
own populations. The main advantage of fungal biocontrol agents is their
high host specificity. Pathogens can distinguish between a crop and a
closely linked parasitic weed, where chemical herbicides have suffered
from low margins of safety. Approximately 30 fungal genera are reported
to occur on Orobanche spp. (Kott 1969; Stankevich 1971; Timchenko
and Dovgal 1972; Taslakh’Yan and Grigoryan 1978; Hódosy 1981; Al-
Menoufi 1986; Bedi and Donchev 1991; Amsellem et al. 1999; Thomas
et al. 1999a; Boari and Vurro 2004).
Results of surveys for fungal pathogens of Orobanche and Striga
revealed that Fusarium species were the most prominent ones associated
with diseased Orobanche and Striga species. F. oxysporum is the pre-
dominant species. Fusarium species as soil-borne fungi possess several
advantages that render them suitable for the bioherbicide approach. The
saprophytic nature of Fusarium spp. allows them to be cultured in liq-
uid as well as solid media; the formae speciales of F. oxysporum are
highly host-specific. Because most of the damage to host crops occurs
while the parasitic weed is still underground, use of soil-borne biocon-
trol agents such as Fusarium spp. can add to improving crop yield by
destroying the parasite at its early developmental stages. To date about
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17 Fusarium species are reported to be associated with either Orobanche

or Striga. When tested under controlled and/or field conditions, six
Fusarium species (F. arthrosporioides, F. nygamai, F. oxysporum, F.
oxysporum f.sp. orthoceras, F. semitectum var. majus, F. solani) have
shown significant disease development in selected species of Orobanche
(Kott 1969; Nalepina 1971; Timchenko and Dovgal 1972; Panchenko
1974; Hódosy 1981; Al-Menoufi 1986; Bedi and Donchev 1991; Thomas
et al. 1998, 1999a; Amsellem et al. 2001a; Müller-Stöver et al. 2002; Sha-
bana et al. 2003) and in selected species of Striga (Abbasher and Sauer-
born 1992; Ciotola et al. 1995, 2000; Abbasher et al. 1996; Kroschel et
al. 1996; Sauerborn et al. 1996a; Hess et al. 2002; Marley et al. 2004).
All growth stages from ungerminated seeds up to flowering stalks can
be attacked (Sauerborn et al. 1996b, Thomas et al. 1999b). Consequently,
seeds of Orobanche and Striga may be infected by the application of
Fusarium spp. even if no host plant for the parasite is present in the field.
That means that the parasite seed bank could be lowered every season.
A successful application of this strategy would add advantages to the
bioherbicide approach. However, much research is still needed in order
to develop Fusarium spp. as a biocontrol agent against the seeds of these
parasites.
Under laboratory and greenhouse conditions excellent control was
repeatedly observed with F. oxysporum f.sp. orthoceras against O.
cumana on sunflower (Shabana et al. 2003; Müller-Stöver et al. 2004).
Amsellem et al. (2001b) and Cohen et al. (2002a) observed reduction in
O. aegyptiaca attached to tomato in greenhouse experiments using host-
specific strains of F. oxysporum and F. arthrosporioides.
Although data on the efficiency of Fusarium spp. to control
Orobanche in the field are rare, the results already indicate that Fusar-
ium spp. in most cases do not provide the level of control desired by
farmers. Thus, so far there has been a lack of success with the present
means for potential inundative bioherbicides for biocontrol of the root
parasitic weeds.
Novel Approaches. A novel approach, aimed to increase the level of con-
trol, is to use a “multiple-pathogen strategy” (Charudattan 2001) where
two or more pathogens are combined and applied before or after para-
site emergence. The feasibility of this approach has been demonstrated
in the control of O. cumana in sunflower (Dor et al. 2003). A bioherbi-
cide system was based on two fungal pathogens, F. oxysporum f. sp.
orthoceras isolated from O. cumana on sunflower and F. solani isolated
from O. aegyptiaca on tomato. In pot trials, the pathogens gave a low
control level when used individually but when applied as a mixture,
04_4696.qxd 10/25/06 2:20 PM Page 313
both fungi caused a significant reduction of the number of emerged O.

cumana and of the parasite’s dry weight.
Recently it was shown that systemic acquired resistance (SAR) of host
plants can be used for the control of agronomic important Orobanche-
species (Sauerborn et al. 2002; Gonsior et al. 2004, Pérez-de-Luque et al.
2004). After application of the resistance inducing agent BION® (1,2,3-
benzothiadiazole-7-carbothioic acid S-methyl ester, Syngenta) the pro-
duction of defence mechanisms is stimulated in host roots enabling this
host plant to protect itself more efficiently to parasitism of Orobanche.
Müller-Stöver et al. (2005) have shown successful control of O. cumana
when the resistance inducer Benzothiadiazole (BTH) was integrated
with the bioherbicidal pathogen F. oxysporum f. sp. orthoceras. The
combined treatment of the two agents resulted in highly reliable control
of O. cumana and reduced the parasite’s emergence up to 100%. The
excellent control level in the combined treatments resulted in a lower
number and dry weight of O. cumana shoots. This indicates that the
combination of control strategies takes effect already in the early devel-
opmental stages of the parasite. This could either be due to an enhanced
activity of the fungus against the early underground stages of the para-
site or to an enhanced induced resistance within the sunflower plants.
However, no enhancing effects of BTH on virulence and growth of the
fungus have been observed in laboratory experiments.
Another approach, which receives increasing attention, is the engi-
neering of hypervirulence genes into weed-specific pathogens, e.g.,
genes that encode enzymes that degrade metabolites involved in crop
defense mechanisms such as phytoalexines, or coding for enhanced vir-
ulence by the production of fungal toxins (Gressel 2002; Gressel et al.
2004). To enhance virulence two Fusarium species that attack
Orobanche have been transformed with two genes of the indole-3-
acetamide pathway that convert tryptophan into the plant hormone
indoleacetic acid (IAA) (Cohen et al. 2002b). Overproduction of IAA pro-
vided a slight increase in virulence compared to the wild type but not
enough to attain a satisfactory level of control. Extreme care should be
taken with such genetically modified organisms due to their possible
environmental impact, and fail-safe mechanisms should be installed
and tested prior to release into the environment. Some possible fail-safe
mechanisms are discussed by Gressel (2001, 2002).
5. Artificial Resistance. The potential of artificial resistance in crops,

based on the power of biotechnology and plant genomics, makes a
genetic engineering strategy viable. Recent advances in understanding
04_4696.qxd 10/25/06 2:20 PM Page 314

the biology of parasitism offer opportunities for using this approach to

enhance the control of these weeds (Westwood 2004).
The development of genetically engineered herbicide-resistant crops
allowed the control of Orobanche on these crops with the help of the
respective herbicides. This was based on the hypothesis that transgenic
crops, with herbicide resistance due to a modification of the target site
of the herbicide, would allow the systemic translocation of the unme-
tabolized herbicide to the attached parasite. A nearly complete control
of broomrape was consequently achieved with model transgenic crops
bearing genes for target-site resistances to glyphosate, asulam, and ALS
inhibitors (Joel et al 1995a). Loading seeds of these transgenic crops with
the respective herbicides was also effective in the control of the parasite,
at least in early stages of the crop growth (Joel et al. 1999).
Crop plants with an artificial Orobanche resistance are only now grad-
ually emerging, opening new horizons by extending the sources of resis-
tance further to the very limited number of natural resistance resources
that have so far been found. Beside the advantages of this technology,
some disadvantages to artificial resistances may, however, arise, since
expression of novel genes in crop plants could pose “food safety” issues.
Concern may also arise regarding the possible gene transfer from trans-
genic crop plants to wild plants. Strategies to avoid this danger are fully
discussed by Gressel (2002).
Two main strategies may be envisaged for the development of artifi-
cial resistance: (1) silencing of key metabolic genes in the parasite; and
(2) development of local resistance in the host, either by allowing the
host to use its resistance mechanisms like hypersensitive reaction (HR)
against the parasite, or by providing it with a toxin that may selectively
control the parasite.
Silencing. The silencing approach has already been demonstrated as an
effective control method against nematodes and viral disease (Atkinson
et al. 2003). Since the silencing-signal can move in the plant, even across
the graft union (Palauqui et al. 1997), and since the connection between
Orobanche and its hosts includes direct phloem continuity (Dörr and
Kollmann 1995), one may hypothesize that a silencing-signal would
also move from host to parasite, and could thus serve as a resistance
agent. This may be accomplished by generating transgenic host plants
harboring constructs generating siRNA of the Orobanche target gene.
Artificial Resistance. The development of an artificial local resistance
against Orobanche requires two major elements: (1) genes whose prod-
ucts may provide resistance, and (2) promoters that target the expression
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of such genes to the infection area. The first reports regarding the con-
struction of an artificial Orobanche resistance in plants have utilized the
gene encoding Sarcotoxin IA (Aly et al. 2005). Sarcotoxin IA is a pep-
tide of the cecropin family, that was isolated from the flesh fly Sar-
cophaga peregrina (Kanai and Natori 1989) and was formerly used to
provide resistance against pathogenic bacteria. Cecropin primary effect
is the disruption of microbial membranes (Natori 1995). The selectivity
of these toxins toward bacteria is attributed to the high level of posi-
tively-charged residues on the hydrophilic end of the peptide, causing
it to associate preferentially with bacterial membranes that carry a more
negative charge than eukaryotic cells (Shai 1999). Because cecropins tar-
get membranes rather than specific receptors, they are effective against
a wide range of bacteria (Aly et al. 1999) and have been recognized as
potentially useful tools in enhancing plant resistance to microbial
pathogens. Transgenic tobacco expressing sarcotoxin IA under control
of either constitutive (E12W) or inducible (PR-1a) promoters showed
enhanced resistance to bacterial and fungal pathogens (Mitsuhara et al.
2000; Ohshima et al. 1999). Assuming that the mechanism of sarcotoxin
IA toxicity to Orobanche is membrane disruption, it was hypothesized
that the peptide may be translocated from host to parasite following the
strong sink produced by the parasite.
Initial studies indicated that sarcotoxin IA peptide synthesized by
yeast (Saccharomyces cerevisiae) (Aly et al. 1999) inhibited O. aegypti-
aca seed germination and radicle elongation. Based on this study, Aly
et al. (2005) showed for the first time enhanced resistance to O. aegyp-
tiaca when the sarcotoxin IA gene was linked to the constitutive root-
specific Tob promoter to generate sarcotoxin-expressing tomato plants.
Observations of parasite growth in association with these plants indi-
cated that parasites were able to attach to the host root, but grew abnor-
mally and had an increased mortality rate. In the absence of Orobanche,
growth and development of crops expressing sarcotoxin was equal to
that of nontransformed plants, suggesting that low levels of sarcotoxin
peptide are not detrimental to the host plants. However, Orobanche
resistance in these plants was incomplete. Therefore, it was proposed to
increase the efficacy of sarcotoxin by regulating its expression with the
more specific HMG2 promoter (Cramer et al. 1993), which has previously
shown a strong and sustained expression in host roots at the site of
Orobanche entry (Westwood et al. 1998). The expression pattern of the
HMG2 promoter in response to O. aegyptiaca represents many advan-
tages of an optimal promoter for engineering resistance: (1) its expres-
sion is induced immediately following parasite penetration of the host
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root; (2) it occurs specifically in the area immediately surrounding the

point of attachment; and (3) its expression continues throughout devel-
opment of the parasite (Westwood et al. 1998).
Transgenic tobacco plants harboring the sarcotoxin IA gene, under the
regulation of HMG2 showed enhanced resistance to Orobanche result-
ing in higher numbers of aborted parasitization events, a reduced
Orobanche biomass, and a greater host biomass following parasite inoc-
ulation (Hamamouch et al. 2005). Protein stability may be the most crit-
ical limiting factor because sarcotoxin IA is subject to rapid degradation
in plants from extracellular proteases (Okamoto et al. 1998). Therefore,
more research is needed to understand the mechanism of sarcotoxin IA
selectivity toward Orobanche, and to optimize this mechanism for engi-
neering parasite-resistant crop plants. The current biotechnological
developments should make this approach easier and more fruitful
through identification of other parasite-responsive gene promoters, and
the choice of additional genes that could be useful in engineering
induced resistance against Orobanche and other parasitic weeds.
6. Integrated Orobanche Management. Integrated Orobanche manage-

ment suggests the use of two or more control methods for managing the
parasite in a particular field. Taking into account the present status of
each of the control measures described above, the most practical and fea-
sible combination would be the use of resistant cultivars together with
chemical control or hand weeding. The main obstacle in using resistant
cultivars is their fast breakdown and the appearance of new aggressive
populations of the parasite. This process may probably start with only
one or a few individual events of individual Orobanche seeds that ger-
minate and succeed in parasitizing the resistant crop, complete their
development, and set seeds. The proportion of its offspring in the seed-
bank will increase each time the resistant variety is grown in the field,
until the resistant variety is heavily attacked and can no more be
regarded resistant. In order to prevent this set of events, the use of resis-
tant cultivars should always be accompanied by other control methods
that should eliminate seed production and dispersal by the individual
parasites that bypass the resistant mechanism of any resistant crop cul-
tivar. This means that chemical control or hand weeding should be per-
formed toward the end of the season before Orobanche seed dispersal,
even in cases in which only few individual parasites develop in the field.
A similar approach should also be adopted in the absence of crop
resistances, when chemical control seems to be successful for a partic-
ular parasite. In this case, hand weeding would help in eliminating the
rare (but potentially existing) parasite individuals that survive follow-
04_4696.qxd 10/25/06 2:20 PM Page 317
ing the chemical treatment and that would otherwise propagate and
jeopardize the efficacy of the herbicide.
Wisely combining these three control methods would significantly
reduce or even completely prevent resistances from breaking down.
Other control methods that are also discussed in this section are still in
a premature state and are not efficient enough for commercial use. Much
research should be invested in each one of these methods in order to
allow their application as part of a practical integrated Orobanche
management.
C. Striga Management
Striga spp. are difficult to manage as they emerge after normal weeds have
been controlled in the field, do most of their damage while they are still
underground, and produce copious amounts of seed that can remain
viable in the soil for many years. Therefore, Striga management strategies
are quite distinct from those used to control other weeds. In order to be
adopted by farmers, management practices must not only be effective in
controlling Striga and in reducing Striga related yield losses, but must be
compatible with the circumstances of the intended beneficiaries.
Striga spp. are pests of cultivated crops primarily in Africa and the
vast majority of farmers are subsistence level. Most of the food they pro-
duce is consumed by the farm family with little, if any, sold for cash.
Subsistence farmers use limited purchased inputs, have little flexibility
in the choice of crop, employ labor intensive rather than input intensive
practices, and are generally risk adverse with no safety net if they fail.
Furthermore, African farmers generally have limited access to informa-
tion on how to confront the Striga problem due to the low level of for-
mal education and poor rural infrastructure. These circumstances make
the development and adoption of effective management practices for this
pernicious pest even more challenging.
As a result of decades of research and farmer experience, a range of
Striga management practices have been developed that can be broadly
classified into the general themes of containment, chemical, biological,
and cultural control, and host plant resistance.
1. Containment. Significant areas within agro-ecologies that are suitable

for Striga growth are currently free of Striga such as the Central and East-
ern Province of Kenya (Hassan and Ransom 1998). Furthermore, many
farms and even fields within a farm can be virtually Striga-free in nom-
inally Striga infested areas. Preventing the movement of Striga into
uninfested areas will in most cases require significantly less resources
04_4696.qxd 10/25/06 2:20 PM Page 318

than controlling it once it is well established. Containment was a key ele-

ment in the Witchweed Eradiation Program in the US (Sand and Man-
ley 1990). There have been few studies of the factors involved in the
spread of Striga seed, but human aided movement is the most likely
cause of new infestations. Berner et al. (1994b) found significant quan-
tities of Striga seed associated with crop seeds sold in local Nigerian
markets. The movement of sugar company-provided tractors between
farms of different growers was suggested as one of the reasons why
Striga is so widespread in the sugar growing areas of western Kenya
(Ransom 1996). In the US, long distant movement of Striga seed was
reported to be associated with contaminated farm and earth-moving
equipment and commodities (Sand and Manley 1990).
Containment of Striga asiatica in the Carolinas in the US was achieved
through a regulatory program that included a strict quarantine of all land
that was found to be infested (Sand and Manley 1990). Though many
aspects of the successful regulatory program in the US would seem to
be logistically difficult to implement in Africa, educating farmers on the
use of clean seed, and avoiding the use of tools and equipment from
neighboring farms that are known to be contaminated with Striga seed
should be doable and would help contain the spread of Striga (Ransom
1996).
Once a field is infested with Striga, controlling its seed production is
problematical. Parker and Riches (1993) estimated that 58,000 seeds
can be produced by a single plant of S. asiatica and 200,000 by S. her-
monthica. The only method for controlling seed production that is avail-
able in subsistent systems is hand weeding. Nevertheless, hand weeding
is not widely practiced in most of Africa, probably because of the lim-
ited immediate return from the practice and the tediousness of the task
(Ransom 2000). Reducing established seedbanks requires a long-term
commitment, but as few as two or three flowering Striga plants per
square meter is reported to be sufficient to maintain seed numbers in the
soil at damaging levels (Van Delft 1997).
2. Chemical Control. Currently, there is virtually no use of herbicides

in the small-scale subsistence farming sector of Africa, as farms are
small and most weeds are adequately controllable through hand weed-
ing. Recommendations for herbicides for the control of Striga and of
potential hosts of Striga in nonhost crops were developed as part of the
Witchweed Eradiation Program in the US (Langston and English 1990).
A number of herbicides, particularly 2,4-D, effectively controlled
emerged Striga in crops and stopped Striga reproduction, but were
largely ineffective in reducing Striga related yield losses. Dicamba
04_4696.qxd 10/25/06 2:20 PM Page 319
applied to maize provided some protection when applied before the

emergence of Striga (Odhiambo and Ransom 1993) but timing of appli-
cation is critical both in terms of crop safety and Striga control. Aliyu
et al. (2004) reported yield improvements in Striga-infested fields with
a preemergence application of metolachlor and prometryne followed by
acifluorfen post-emergence.
Ethylene. Ethylene induced germination of conditioned Striga seed
(Egley and Dale 1970) and became the key control technology of the suc-
cessful S. asiatica eradication program in the USA (Egley et al. 1990).
There has been no serious effort to promote the use of ethylene in Africa
due to the inherent logistical challenges associated with its application.
Moreover, there has been very limited published research conducted in
Africa to demonstrate the effectiveness of ethylene on S. hermonthica.
In East Africa, the amount of ethylene-induced suicidal germination S.
hermonthica was in the range of 60 to 80% (Ransom and Njoroge 1991),
compared to ~90% Striga asiatica germination in the US (Egley et al.
1990). Odhiambo and Ransom (1996) found that even after four seasons
of application, ethylene did not completely control Striga in a continu-
ous maize cropping system. Data from West Africa suggest that unlike
S. asiatica in the US, there can be a significant level of dormancy in S.
hermonthica (Gbèhounou 1998). Ethylene can only stimulate suicidal
Striga germination of seeds that are nondormant, that are conditioned
and otherwise ready to germinate. Given the impact that ethylene has
had in the eradication of Striga from the US, additional research and
development efforts on the use of ethylene for the control of Striga in
Africa seems to be justified.
Seed Dressing. A promising approach to the control of parasitic weeds
is herbicide seed priming that consists of soaking crop seed in a herbi-
cide solution such that the herbicide is later present in the crop seedling
to inhibit growth of attaching parasites (Joel et al. 1997b; Gressel and Joel
1998). This technique is effective where selectivity exists between crop
and parasite; for example, varieties of imidazolinone-resistant maize.
The treatment of cowpea seed with imazaquin was suggested for the con-
trol of S. gesnerioides and Alectra vogelii (Berner et al. 1994a), and a sim-
ilar approach is also currently tested for the control of S. hermonthica
in sorghum and pearl millet (Pennisetum glaucum L.) (Dembélé et al.
2005), illustrating both the potential and limitations of adapting seed
priming technology.
Based on research with Orobanche (Joel et al. 1995a), herbicides
applied to transgenic herbicide resistant maize at the time of Striga
attachment has promise in controlling Striga and in protecting crop
04_4696.qxd 10/25/06 2:20 PM Page 320

plants from Striga-related yield losses. Current policies, however, restrict

the use and testing of transgenic crops in most African countries.
The development of maize hybrids with nontransgenic resistance to
ALS inhibiting herbicides recently provided new options for the devel-
opment of herbicide-based systems that target Striga control in Africa.
A number of ALS-inhibiting herbicides applied to the seed of maize
hybrids with tolerance to ALS-inhibiting herbicides effectively con-
trolled Striga (Abayo et al. 1998; Berner et al. 1997). Of the initially
screened herbicides and methods of application, imazapyr and
pyrithiobac dressed to the maize seed were the most active against
Striga, probably due to their relatively long persistence in the rhizos-
phere (Kanampiu et al. 2001, 2002a). Multilocation testing demonstrated
that this herbicide system provided excellent early season control of
both S. asiatica and S. hermonthica and could increase yield three to
fourfold in heavily infested fields (Kanampiu et al. 2003). Furthermore,
this system permits intercropping with other crops, such as cowpea, as
long as the intercrop is planted at least 15 cm from the point where the
maize seed is planted (Kanampiu et al. 2002a). This technology appears
to be compatible with the current circumstances and practices of
smallscale farmers in Africa in that the herbicide is applied to the seed
(potentially by a seed company) so no special application equipment or
calibration is needed, the rates are low and cost-effective for areas that
are heavily infested by Striga, and it does not interfere with commonly
used intercropping practices. There is potential for Striga to develop
resistance to ALS inhibitors, and resistance strategies need to be
employed from the initial release of this technology in order to prolong
its utility (Gressel et al. 1996).
3. Host Plant Resistance. Crop cultivars with resistance to Striga have

long been proposed as a cost-effective method of reducing Striga-related
losses that would be compatible with the low-input systems of African
farmers. Cowpea cultivars that are resistant to selected strains of S. ges-
nerioides have been found and resistant genes exploited in breeding
programs (Lane et al. 1993, 1994a). Complete resistance to Striga by sus-
ceptible cereal crops, however, has yet to be found, though considerable
variability for the level of Striga attack and tolerance to Striga parasitism
has been reported both between and among the most commonly para-
sitized cereals. This partial resistance or tolerance has been attributed
to a number of different mechanisms including: rooting patterns that
allow some level of avoidance (Ransom and Odhiambo 1995; Cherif-Ari
et al. 1990); production of reduced levels of Striga germination stimu-
lants (Ejeta and Butler 1993); increased photosynthetic rate (Gurney et
04_4696.qxd 10/25/06 2:20 PM Page 321
al. 2001); and growth and development features that delay attachment
(Gurney et al. 1999). Cultivars with improved resistance/tolerance to
Striga have not been widely adopted because they are poorly adapted,
have low yield potential (Oswald and Ransom 2004) or do not possess
other traits valued by farmers such as plant height and grain character-
istics (Ezeaku and Gupta 2004).
Identifying sources of resistance and breeding for resistance is a com-
plex process that requires special methodologies to ensure good progress
(Haussmann et al. 2000b; Omanya et al. 2004). Biotechnology offers
new approaches and tools for improving the level of resistance in
adapted genotypes. Molecular markers have been identified for the
mechanical-type resistance found in the sorghum N13 (Haussmann et al.
2004) and are being used to improve resistance in farmer-preferred cul-
tivars. Biotechnology may also facilitate the incorporation of genes from
wild relatives, e.g. Tripsacum spp. genes into maize (Gurney et al. 2003).
Mutations induced with transposons have shown promise in producing
genotypes with resistance to Striga in maize (Grimanelli et al. 2000).
Gressel (2000) has proposed dispersing deleterious transposons in weed
populations as a way of controlling Striga.
Control based largely on host-plant resistance is imperative for use in
subsistence agriculture. A Striga-resistant cultivar supports significantly
fewer Striga plants and has a higher yield in the presence of Striga than
a susceptible cultivar (Ejeta and Butler 1993). Tolerant cultivars support
almost as many Striga plants as do susceptible hosts but without a pro-
portionate reduction in crop productivity. On the other hand, immune
genotypes would be totally free of Striga when grown under varying
infestation levels, but such cultivars have not been found in crop plants.
Overall, there appears to be real paucity of sources of resistance to Striga
and similar weedy root parasites in most crop plants. Yet, through the
persistent efforts of plant breeders and agronomists, crop varultivars
with varying levels of resistance to Striga spp. have been reported in sev-
eral crops, including cowpea (Atokple et al. 1995), maize (Kling et al.
2000), rice (Johnson et al. 1997), and sorghum (Olivier et al. 1991b; Ejeta
et al. 2000).
Conventional breeding for Striga resistance in crop plants has gener-
ally been frustrating. Plant breeding methods that work well for improv-
ing other desirable crop characteristics have not operated at the same
efficiency for Striga resistance (Ejeta and Butler 1993). Species speci-
ficity is contributing to the slow progress in improving Striga resis-
tance, that is, a crop showing resistance to one species of Striga may be
susceptible to another. Even more frustrating are intraspecific varia-
tions in the parasite to the degree that an acceptable level of resistance
04_4696.qxd 10/25/06 2:20 PM Page 322

to one physiological strain or ecotype of S. hermonthica, for instance,

may not hold when the crop is grown in the presence of different S. her-
monthica populations. By the very nature of the plant with plant asso-
ciation there may be a lack of resistance options for the host against
plant parasites relative to more distantly related pests (Pennings and
Calaway 2002). Finally, the lack of rapid and efficient screening tech-
niques retards the resistance breeding progress. Field measure of Striga
resistance, most commonly emergence counts, represents a sum total
of the entire parasitic association and is therefore a quantitative trait
with polygenic inheritance. Numerous environmental effects and
genetic variability of parasite populations confound the field screening
process.
4. Cultural Management Practices. Cultural management practices that

have been developed and recommended include rotations, soil fertility
enhancement, and transplanting.
Crop Rotation. Rotating susceptible cereal crops with crops that are
nonhosts to Striga, particularly those that act as false hosts (i.e., crops
that stimulate Striga to germinate but are not themselves parasitized),
has long been advocated as a simple way of reducing Striga seed levels
in the soil. Recent research has demonstrated that a wide range of rota-
tions can be effective in reducing Striga numbers and increasing yields
in a subsequent cereal crop (Odhiambo and Ransom 1994; Carsky et al.
2000; Sauerborn et al. 2000; Oswald and Ransom 2001; Schulz et al.
2003; Ahonsi et al. 2004; Hess and Dodo 2004). Berner et al. (1995) rec-
ommend crop rotations with selected nonhost cultivars that are effica-
cious in germinating Striga seed as the central focus of an integrated
Striga control program. Ransom (2000) and Oswald and Ransom (2001),
however, suggest that selection of rotational crops should be based on
socioeconomic considerations (market value and availability) and not
just on the biological potential to induce Striga germination. The lack
of adoption of rotations as a means to reduce Striga has been minimal
in many subsistence cereal-based farming systems primarily because of
the reluctance of farmers to reduce the amount of land planted to their
staple cereal crop. Oswald et al. (1999) found that after extensive demon-
strations of a range of Striga control on farm options, rotation was
selected as the third choice after intercropping and catch cropping, even
though it was technically superior to the others. There is justification for
continued adaptive research to identify nonhost crops that fit in rota-
tions with cereals, and in identifying markets and extending production
information about them to farmers in order to promote their use. Devel-
04_4696.qxd 10/25/06 2:20 PM Page 323
oping ready and stable markets for alternative crops may have a greater
impact on the adoption of rotations than biological effectiveness per se.
Managed or planted fallows, where fast growing nitrogen-fixing non-
crop species are grown for one or more seasons to help improve subse-
quent cropping productivity, is being promoted as a means of improving
nutrient-depleted fields (Buresh and Cooper 1999). Some species, (e.g.,
Sesbania sesban (Linn.) Merrill., Senna siamea Irwin & Barnaby, and
Leucaena leucocephala (Lam.) de Wit.) used in a managed fallow sys-
tem nearly eliminated Striga asiatica development in a subsequent
maize crop (Kwesiga et al. 1999). Widespread adoption of managed fal-
lows as a means of Striga control will be constrained by lack of seed,
increased labor requirement, and the fact that there is no crop harvested
during the fallow period. These factors were found to also constrain the
adoption of cover crops in Africa (Morse and McNamara 2003).
Transplanting. Older crop plants have been shown to be more resistant
to, and less damaged by, Striga than young seedlings (Cechin and Press
1993; Dawoud et al. 1996). Transplanting has been developed as a
method of avoiding early season attack. Oswald et al. (2001) found
increased maize yield and reduced Striga parasitism when transplanted
maize seedlings (at least 17 days old) were compared to the direct seeded
control. Later maturing maize cultivars benefited more from trans-
planting than earlier maturing ones (Oswald and Ransom 2002). Trans-
planting has also been tried with other crops (Gbèhounou et al. 2004)
with some success, though Oswald et al. (2001) found establishing trans-
planted sorghum more difficult than maize. Constraints to the use of
transplanting for Striga control include the high cost of labor and the
necessity that nurseries be established near sources of water. Trans-
planting maize in order to intensify land use is practiced on more than
100,000 ha annually in the Red River delta of Vietnam where labor is less
constraining and land more limiting (Maranthee 1991). Transplanting
crop plants for Striga avoidance is also labor intensive, but Oswald and
Ransom (2001) found it to be profitable to farmers if Striga levels were
very high in only one in three seasons.
Soil Fertility Enhancement. It has long been recognized that Striga is
most problematic on soils with low fertility, particularly those that are
low in nitrogen. Pieterse and Verkleij (1991), however, in their review
of the literature found that although applying N fertilizer does reduce
Striga emergence consistently, it was not possible to conclude that Striga
could be controlled simply by managing soil fertility. Given the nutri-
ent depleted status of most of the intensively cropped soils in Africa,
restoring productivity to most Striga infested farms in Africa requires
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addressing the Striga and soil infertility problems concurrently. Ransom

(1999) reported that after three or four seasons, maize yields could be
doubled by hand weeding Striga or by applying N fertilizer, and quadru-
pled when both N and hand weeding were applied. Much of the current
soil fertility-related research is directed toward developing cost-effective
ways of improving soil fertility by using biological nitrogen fixation, (i.e.,
rotations or planted fallows with legumes as described above).
Enhancing the natural rate of Striga seed demise can be increased by
altering the fertility status of the soil (Sauerborn et al. 2003). Ransom
(1999) found that with continuous incorporation of maize stover and the
addition of inorganic N in sufficient quantity to maintain a carbon :
nitrogen ratio that was favorable to microbiological activity, Striga seed
numbers in the soil declined over time, even with new additions of seed
from uncontrolled Striga. Ahonsi et al. (2004) found that crop rotation
with soybean, and the addition of N, P, or NPK fertilizers directly
enhanced the suppression of Striga in the soil. Enhancing the rate of
Striga suppressiveness with fertilizers and organic inputs may have
limitations in the drier environments, where microbial activity is lim-
ited by moisture and not carbon and nitrogen (Ransom 1999).
5. Biological Control. There are a number of insects and diseases that can
affect the growth and fecundity of Striga spp. (Berner et al. 2003). Nev-
ertheless, classical and inundative biological Striga control approaches
with insects have met with limited success (Kroschel et al. 1999). Sev-
eral insect species (i.e. Smicronyx spp. and Junonia orithya), however,
routinely reduce the amount of new Striga seeds being produced in
some locations and years (Kroschel et al. 1995, 1999; Traore et al. 1996)
and are important as a component of an integrated Striga control pro-
gram.
About 16 fungal genera are known to be found on Striga spp. (Meis-
ter and Eplee 1971; Zummo 1977; Greathead 1983; Abbasher and Sauer-
born 1992; Kirk 1993; Ciotola et al. 1995; Abbasher et al. 1995, 1998;
Kroschel et al. 1996; Marley et al. 1999; Hess et al. 2002). Strains of
Fusarium oxysporum were identified that are highly pathogenic to all
development stages of Striga (Ciotola et al. 1995; Kroschel et al. 1996).
Selective strains have been formulated as mycoherbicides that have
been effective in controlling Striga and in many cases increasing crop
yields (Ciotola et al. 2000; Marley et al. 2004). Trials to evaluate Fusar-
ium species pathogenic on S. hermonthica performed well under con-
trolled conditions. The application of strains of F. nygamai and F.
oxysporum caused more than 90% reduction of S. hermonthica emer-
04_4696.qxd 10/25/06 2:20 PM Page 325
gence (Abbasher and Sauerborn 1992; Ciotola et al. 1995). A major chal-
lenge of this technology is its delivery to the farming community as it is
nonproprietary and has no significant commercial backing. To address
this, techniques for increasing and applying Fusarium spores in ways
that are compatible with the circumstances of farmers in Africa are
being developed. These include using locally available substrates (i.e.,
sorghum straw), inoculating fields by coating sorghum seeds prior to
planting (Ciotola et al. 2000) and developing formulations (i.e., Pesta
granules), with extended shelf life (Elzein et al. 2004).
The bacterium Pseudomonas syringae produces sufficient ethylene to
induce suicidal germination of Striga seed (Berner et al. 1999). In pot
studies, Ahonsi et al. (2003) found that by coinoculating soybeans or
cowpea crops with P. syringae and the nitrogen-fixing bacteria Bradyrhi-
zobia japonicum, Striga development on the following maize crop was
reduced and the maize crop growth was increased, presumably because
of increased demise of Striga seed in the soil during the legume crop-
ping cycle.
Soils which naturally suppress the build up of Striga have been widely
reported (Gbèhounou et al. 1996; Ransom 2000; Berner et al. 1996; Odhi-
ambo and Ransom 1994). The causal factors involved in these soils have
not been elucidated, but suppressiveness is associated with the activity
of microorganisms (Pieterse et al. 1996; Ahonsi et al. 2004). Improved
soil fertility, additions of organic matter, and rotations were found to
increase the natural Striga suppressiveness of soils (Ransom 2000; Sauer-
born et al. 2003; Ahonsi et al. 2004).
Mycorrhiza. With arbuscular mycorrhizal (AM) fungal inoculation, a sig-

nificant reduction in the number of S. hermonthica shoots was noted
(30% in maize and more than 50% in sorghum, Lendzemo et al. 2005),
with an increased crop growth. Similarly, Gworgwor and Weber (2004)
found that Striga emergence in sorghum was significantly reduced by the
mycorrhyza fungus G. mosseae, and that the growth and total dry mat-
ter yield of sorghum increased compared with other AM fungi and to the
control. These studies indicate that AM fungi have the potential to
reduce damage by S. hermonthica to sorghum. AM fungi are therefore
potentially useful for soil management in Striga-infested areas.
With the recent discovery of the role of strigolactones (the Striga ger-
mination stimulants) in promoting AM development, one may suggest
a direct causal relationship between the two phenomena, i.e., for exam-
ple, down-regulation of mycorrhizal branching factor formation (strigo-
lactones) after mycorrhizal colonization (Matusova et al. 2005).
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Perspective. A major constraint to the use of bioherbicidal pathogens

may result from the regulatory authorities in the countries where
Orobanche and Striga are a problem. Since bioherbicidal pathogens are
living organisms, regulators are fearful to introduce them from foreign
countries. In such situations, biocontrol agents probably fail to be mar-
keted internationally. Instead, host-specific strains of fungi have to be
detected in each country and need to be developed independently into
a bioherbicide. However, the prime concern remains enhancing the effi-
cacy of the biocontrol agents currently investigated by fermentation,
formulation, and application technology.
6. Integrated Striga Management. The various Striga management prac-

tices reviewed above offer varying levels of Striga control depending on
the environment in which they are employed, but none currently pro-
vides complete control. Furthermore, the adoptability and utility of
each can vary considerably depending on the farming system and the cir-
cumstances of the farmer. An integrated Striga management approach
currently offers the best possibility for impact at the farm level. Adap-
tive and on-farm research can play an important role in identifying the
most effective mix of component practices; no single mix of practices is
likely to have application across the broad range of environments in
which Striga is problematic. Ransom (1996) suggests combining prac-
tices that reduce seed bank (i.e., hand weeding, suppressive soils, and
rotations) with management practices that maintain or improve the farm
productivity (i.e., seed-dressed imazapyr, inorganic and organic fertil-
izers, use of nonhost crops, and host plant resistance). Berner et al.
(1995) suggest crop rotation with highly effective trap crops as the key
component of an integrated Striga control program. Schulz et al. (2003)
found that growing a resistant maize genotype following a soybean trap
crop increased yield by 80%. For fields with very high levels of infes-
tation, integrating practices that protect yield such as mycoherbicides
and imazapyr applied to herbicide resistant maize hybrids combined
with the most resistant cultivars available show promise (Kanampiu et
al. 2003; Marley et al. 2004). Aliyu et al. (2004) found that combining
herbicides with high yielding tolerant maize cultivars was more prof-
itable than the current farmers’ practices. Regardless of the other com-
ponents, the maintenance and improvement of soil fertility through
nutrient cycling, rotations with nitrogen-fixing species and/or the judi-
cious use of fertilizers will be needed to restore and maintain produc-
tivity when and if Striga levels are reduced (Ransom 2000).
04_4696.qxd 10/25/06 2:20 PM Page 327
VI. CONCLUDING REMARKS
Research during the last two decades have dramatically changed our
understanding of mechanisms of parasitism in the Orobanchaceae, and
more so, contributed numerous methods for the control of these weedy
parasites. Though limited in efficacy in many cases, the control meth-
ods available today represent major progress when compared to the lack
of any means for the control of these plants one or two decades ago.
Crops can be protected by resistance, by selective herbicides, by bio-
control agents, and by cultural methods that have not existed before. We
are now also facing an accelerated progress in the genomic and biotech-
nological research that should soon provide important understanding of
some crucial developmental mechanisms in both the parasites and their
host plants. Artificial resistances, based for example on the expression
of specific toxins at the site of infection, or providing the host with
silencing signals that may be transferred to the parasite and inhibit the
expression of key parasite’s metabolic activities, may protect some addi-
tional crops that are hitherto unprotected. These control methods and
others that may come should not divert our understanding of the eco-
logical system in which the crops are grown. Therefore, one needs to dis-
cuss management rather than control, and seriously consider aspects of
sustaining the fields for continuous future cultivation. In order to meet
this necessity, the following principles should carefully be applied:
1. Care should be taken to avoid use of a single control method, and
to avoid monoculture.
2. Sanitation is a key element in keeping ‘clean’ fields uninfested.
3. Several resistances, genetic or transgenic, should be pyramided in
susceptible hosts, to avoid the development of more virulent par-
asite populations.
4. Documentation and mapping of infested areas may assist in
regional management tactics.
5. Decision-support systems, based on understanding the phenology
of the parasite and on diagnostic tools should help in optimizing
the management options and the timing of the various activities
in the field.
6. Both the control of the seedbank in soil and the prevention of
seedbank replenishment should keep the parasite population
under threshold levels of damage.
7. Education and research are two keys for further success in com-
bating these vicious parasitic weeds.
04_4696.qxd 10/25/06 2:20 PM Page 328

On top of these principles, fundamental research on all key aspects of

parasitism should not only lead to a better understanding of this unique
system in the plant kingdom, but also provide new ideas for the devel-
opment of novel methods for parasitic weed control, to increase crop
productivity.
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04_4696.

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Biology and Management of Weedy

G. Ejeta and P. J. Rich

Horticultural Reviews, Volume 33. Edited by Jules Janick

268 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 269

270 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

loss may occur before diagnosis of infection. In spite of intense efforts

II. ECONOMIC IMPACT

Parasitic weeds develop a strong sink, which allows them to remove

A. Weedy Orobanche Species

1. Orobanche crenata Forsk. This parasitic weed, mainly restricted to

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 271

2. Orobanche aegyptiaca Pers. This species is an important pest of

3. Orobanche ramosa L. This species attacks many different crop plants;

272 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

countries. It attacks potato, tomato, eggplant (Solanum melongena L.),

4. Orobanche foetida Poir. This parasitic weed has recently been

6. Orobanche cernua Loefl. This parasitic weed is known in native habi-

7. Orobanche cumana Wallr. This species has specialized as a pest of

8. Orobanche coerulescens Stephan. This parasitic species was reported

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 273

B. Weedy Striga and Alectra Species

274 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

2. Alectra vogelii Benth. This parasite causes considerable yield losses

A. Weedy Orobanche Species

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 275

geographical distribution of the weedy species of Orobanche is mainly

276 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

which is found only in cultivated and disturbed habitats, O. ramosa is

B. Weedy Striga and Alectra Species

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 277

genus Striga includes 50 to 60 species, all of which are said to be para-

278 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

IV. DEVELOPMENTAL ASPECTS

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 279

Fig. 4.1. Life cycle of a weedy root parasite.

and a haustorium is formed. Intrusive cells of the haustorium penetrate

280 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

A. Seed Dormancy and After-Ripening

1. Conditioning. Following seed imbibition a moist environment is

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 281

and developmental process that consists of a series of events, each cru-

2. Germination Stimulation. Parasitic plants of the Orobanchaceae

282 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 283

Additional unrelated compounds that may or may not be present in

284 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

2,6-dimethoxy-1,4-benzoquinone (DMBQ) are active haustorial initiators

E. Attachment and Penetration

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 285

ment, the remaining seed storage lipids are mobilized in S. asiatica

286 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

delayed for 3 to 4 days in S. asiatica, during which further subcellular

F. Further Haustorial Development

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 287

vascular connections with their host. The tubercle of Striga hermonth-

288 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

the findings that net carbon fixation is higher in tobacco infected by O.

4. BIOLOGY AND MANAGEMENT OF WEEDY ROOT PARASITES 289

290 D. JOEL, J. HERSHENHORN, H. EIZENBERG, R, ALY, G. EJETA, P. RICH, J. RANSOM,

turnover of aspargine in the haustoria. By contrast, they found an inten-

H. Seed Production and Dispersal