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Breeding For Resistance To Whitefly-Transmited Geminivirus PDF
Breeding For Resistance To Whitefly-Transmited Geminivirus PDF
(2002), 140:109-127
Printed in Great Britain
109
Department of Virology, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250,
Israel
2
Department of Plant Genetics, Agricultural Research Organization, The Volcani Center, Bet Dagan
50250, Israel
(Accepted 11 March 2002; Received 27 December 2001)
Summary
Geminiviruses comprise a large and diverse family of viruses that infect a wide range of important
monocotyledonous and dicotyledonous crop species and cause significant yield losses. The family
Geminiviridae is divided into three genera, one of which is Begomovirus. Species of this genus are
transmitted by the whitefly Bemisia tabaci in a persistent, circulative manner and infect dicotyledonous
plants. Severe population outbreaks of B. tabaci are usually accompanied by a high incidence of
begomoviruses. During the last two decades, there has been a worldwide spread of the B biotype of B.
tabaci, accompanied by the emergence of whitefly-transmitted geminiviruses. Control measures in
infected regions are based mainly on limitation of vector populations, using chemicals or physical
barriers. However, under conditions of severe whitefly attack, none of these control measures has
sufficed to prevent virus spread. Thus, the best way to reduce geminivirus damage is by breeding
crops resistant or tolerant to the virus, either by classical breeding or by genetic engineering. A number
of begomoviruses have been the subject of much investigation, due to their severe economic impact.
This review considers the most severe viral diseases of four major crops (tomato, bean, cassava and
cotton). The approaches taken to breed for resistance to these viral diseases should provide a perspective
of the issues involved in breeding for begomovirus resistance in crop plants.
Key words: Geminivirus, resistance, breeding, cassava, bean, tomato, cotton, Bemisia tabaci
Introduction
Geminiviruses are a large and diverse family of
viruses that infect a wide range of important crop
species, including both monocotyledonous and
dicotyledonous plants, and cause significant yield
loses. These viruses are characterised by the
geminate morphology of the capsid and by circular
single-stranded DNA (ssDNA) genomes. The family
Geminiviridae is divided into three genera, based
on genome structure, plant host and insect vector
(Fauquet et al., 2000). Species of the genus
Mastrevirus (Maize streak virus as type member)
are transmitted by leafhoppers (Homoptera:
Cicadellidae), have a monopartite genome, and
generally infect monocotyledonous plants. Species
of Curtovirus (Beet curly top virus, BCTV, as type
member) are also transmitted by leafhoppers, have
a monopartite genome, but with a different genetic
organisation from that of the mastreviruses, and
infect dicotyledonous plants. Species of
Begomovirus (Bean golden mosaic virus, BGMV, as
type member) are transmitted by the whitefly
Bemisia tabaci (Gennadius) and infect
dicotyledonous plants. Most begomoviruses of the
Old World and all New World begomoviruses
*Corresponding Author E-mail: lapidotm@netvision.net.il
2002 Association of Applied Biologists
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Fig. 1. Field inoculation of susceptible tomato plants with Tomato yellow leaf curl virus (TYLCV). Tomato plants
susceptible to TYLCV (cv. 5656) were transplanted to the field in September 2001, in an area abundant with whiteflies.
The picture was taken 80 days following transplanting. I = Infected; H = Healthy.
Fig. 2. Tomato yellow leaf curl virus (TYLCV) symptom severity rating in segregating F2 populations. Young (10day-old) tomato seedlings from an F2 population segregating for resistance were inoculated with TYLCV using
viruliferous whiteflies. Symptom development was evaluated 30 days after inoculation according to the following
scale: (0) no visible symptoms, inoculated plants show the same growth and development as non-inoculated plants;
(1) very slight yellowing of leaflet margins on apical leaf; (2) some yellowing and minor curling of leaflet ends; (3)
a wide range of leaf yellowing, curling and cupping, with some reduction in size, yet plants continue to develop; (4)
very severe plant stunting and yellowing, and pronounced cupping and curling; plant growth stops.
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1995).
Two movement proteins, BC1 and BV1, both
encoded by DNA B of bipartite begomoviruses, are
required for viral infectivity and systemic infection
(Sanderfoot & Lazarowitz, 1996). The BC1 MP
mediates viral cell-to-cell movement by increasing
plasmodesmatal size exclusion limits, whereas the
BV1 MP functions as a nuclear shuttle (Noueiry et
al., 1994; Sanderfoot & Lazarowitz, 1996). The first
suggestion that expression of a non-functional BC1
MP by transgenic plants may induce inhibition of
begomovirus movement came from the work of von
Arnim & Stanley (1992), who tested if BC1 MP from
one virus (Tomato golden mosaic virus; TGMV)
could support movement of another virus (ACMV).
To do this, the ACMV AV1 gene (which encodes the
viral CP) was replaced by TGMV BC1 gene. This
recombinant construct was used to inoculate N.
benthamiana plants, together with ACMV B DNA.
The TGMV BC1 MP not only did not supplement
ACMV movement, it actually inhibited it (von Arnim
& Stanley, 1992). Indeed, transgenic tobacco plants
expressing a mutated form of the BC1 gene of
ToMoV showed resistance to this virus as well as to
Cabbage leaf curl virus (CabLCV) (Duan et al.,
1997b). The tobacco plants were transformed with
the wild type form of BC1, which resulted in
transgenic plants expressing viral disease-like
phenotypes. One of the transgenic plant lines had
an asymptomatic phenotype. In this line, the BC1
transgene underwent a spontaneous mutation,
potentially resulting in the production of a protein
from which the 119 C-terminal amino acids were
deleted and 26 amino acids derived from an
unidentified origin were incorporated (Duan et al.,
1997a).
Recently, transgenic tomato plants expressing the
BV1 or BC1 MPs from Bean dwarf mosaic virus
(BDMV) were generated (Hou et al., 2000). The
transgenic plants expressing the BV1 MP appeared
normal, whereas plants expressing the BC1 MP
showed viral disease-like symptoms, although
BDMV induces only a symptomless infection in
tomato. One BC1 transgenic line did not show any
disease-like symptoms. This line expressed a
truncated BC1 protein, following a spontaneous
mutation, which resulted in a deletion in the 3 region
of the gene. Transgenic R0 plants, expressing either
BV1 or BC1, showed a significant delay in the onset
of infection following inoculation with ToMoV. R1
progeny plants also showed a delay in ToMoV
infection, but to lesser extent than the R0 plants (Hou
et al., 2000). These results demonstrate that
begomovirus MPs, similar to RNA viruses MPs, can
be used for development of PDR. However, to date,
the level of resistance induced by begomovirus MPs
is not sufficient for commercial use.
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of Microbiology 47:739-763.
Fokunang C N, Akem C M, Dixon A G O, Ikotun T. 2000.
Evaluation of a cassava germplasm collection for reaction to
three major diseases and the effect on yield. Genetic
Resources and Crop Evolution 47:63-71.
Fondong V N, Thresh J M, Fauquet C. 2000a. Field
experiments in Cameroon on cassava mosaic virus disease
and the reversion phenomenon in susceptible and resistant
cassava cultivars. International Journal of Pest Management
46:211-217.
Fondong V N, Pita J S, Rey M E C, Kochko A de, Beachy R
N, Fauquet C M. 2000b. Evidence of synergism between
African cassava mosaic virus and a new double-recombinant
geminivirus infecting cassava in Cameroon. Journal of
General Virology 81:287-297.
Fregene M, Bernal A, Duque M, Dixon A, Tohme J. 2000.
AFLP analysis of African cassava (Manihot esculenta Crantz)
germplasm resistant to the cassava mosaic disease (CMD).
Theoretical and Applied Genetics 100:678-685.
Fregene M, Angel F, Gomez R, Rodriguez F, Chavarriaga
P, Roca W, Tohme J, Bonierbale M. 1997. A molecular
genetic map of cassava (Manihot esculenta Crantz).
Theoretical and Applied Genetics 95:431-441.
Fregene M, Okogbenin E, Mba C, Angel F, Suarez M C,
Janneth G, Chavarriaga P, Roca W, Bonierbale M, Tohme
J. 2001. Genome mapping in cassava improvement:
challenges, achievements and opportunities. Euphytica
120:159-165.
Friedmann M, Lapidot M, Cohen S, Pilowsky M. 1998. A
novel source of resistance to tomato yellow leaf curl virus
exhibiting a symptomless reaction to viral infection. Journal
of the American Society for Horticultural Science 123:10041007.
Frischmuth T, Stanley J. 1993. Strategies for the control of
geminivirus diseases. Seminars in Virology 4:329-337.
Frischmuth T, Stanley J. 1998. Recombination between viral
DNA and the transgenic coat protein gene of African cassava
mosaic geminivirus. Journal of General Virology 79:12651271.
Garrido-Ramirez E R, Sudarshana M R, Gilbertson R L.
2000. Bean golden yellow mosaic virus from Chiapas,
Mexico: characterization, pseudorecombination with other
bean-infecting geminiviruses and germ plasm screening.
Phytopathology 90:1224-1232.
Gibson R W, Otim-Nape G W. 1997. Factors determining
recovery and reversion in mosaic-affected African cassava
mosaic virus resistant cassava. Annals of Applied Biology
131:259-271.
Hahn S K, Terry E R, Leuschner K. 1980. Breeding cassava
for resistance to cassava mosaic disease. Euphytica 29:673683.
Hahn S K, John C, Isoba G, Ikoutun T. 1989. Resistance
breeding in root and tuber crops at the International Institute
of Tropical Agriculture (IITA), Ibadan, Nigeria. Crop
Protection 8:147-168.
Hanson S F, Maxwell D P. 1999. Trans-dominant inhibition of
geminiviral DNA replication by bean golden mosaic
geminivirus rep gene mutants. Phytopathology 89:480-486.
Hanson S F, Hoogstraten R A, Ahlquist P, Gilbertson R L,
Russell D R, Maxwell D P. 1995. Mutational analysis of a
putative NTP-binding domain in the replication-associated
protein (AC1) of bean golden mosaic geminivirus. Virology
211:1-9.
Hanson P M, Bernacchi D, Green S, Tanksley S D,
Venkataramappa M, Padmaja A S, Chen H, Kuo G, Fang
D, Chen J. 2000. Mapping a wild tomato introgression
associated with tomato yellow leaf curl virus resistance in a
cultivated tomato line. Journal of the American Society for
Horticultural Science 125:15-20.
Hilje L, Costa H S, Stansly P A. 2001. Cultural practices for
125
126
127
Walkey D G A. 1985. Applied Plant Virology. New York: WileyInterscience. pp. 236-242.
Wilson F D, Brown J K. 1991. Inheritance of response to cotton
leaf crumple virus infection in cotton. Journal of Heredity
82:508-509.
Zakay Y, Navot N, Zeidan M, Kedar N, Rabinowitch H,
Czosnek H, Zamir D. 1991. Screening Lycopersicon
accessions for resistance to tomato yellow leaf curl virus:
presence of viral DNA and symptom development. Plant
Disease 75:279-281.
Zamir D, Ekstein-Michelson I, Zakay Y, Navot N, Zeidan
M, Sarfatti M, Eshed Y, Harel E, Pleban T, van Oss H,
Kedar N, Rabinowitch H D, Czosnek H. 1994. Mapping
and introgression of a tomato yellow leaf curl virus tolerance
gene, TY-1. Theoretical and Applied Genetics 88:141-146.
Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape G W,
Robinson D J, Harrison B D. 1997. Evidence that DNA-A
of a geminivirus associated with severe cassava mosaic
disease in Uganda has arisen by interspecific recombination.
Journal of General Virology 78:2101-2111.
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