Plant Disease • 2019 • 103:2153-2170 • https://doi.org/10.
1094/PDIS-03-19-0472-FE
Maria Lodovica Gullino,† Giovanna Gilardi, and Angelo Garibaldi
Centre of Competence for the Agro-Environmental Sector (AGROINNOVA), University of Torino. Largo Paolo Braccini 2, 10095 Grugliasco,
Italy.
Keywords: disease management, fungi and oomycetes, vegetables
The ready-to-eat salad sector, also called fresh-cut or bagged sal-
ads, represents a very interesting example of innovation. According
to the definition given by the International Fresh-cut Produce Asso-
ciation (IFPA 2000), fresh-cut vegetables are products that are min-
imally processed—only washed, cut, mixed, and packed—to offer
consumers high nutrition, convenience, and flavor while still main-
taining freshness.
Since their origin in Europe in the early 1980s, they have become
more and more common in consumers’ market baskets. The innova-
tion represented by this sector involves the technologies adopted in
growing, processing, and marketing. Agronomists, microbiologists,
chemists, and food engineers are working to provide new solutions to
enhance quality and safety attributes. In most countries, several large
firms share most of the market, followed by a number of private label
†
Corresponding author: M. L. Gullino; marialodovica.gullino@unito.it
Funding: This research has received funding from the European Union’s Ho-
rizon 2020 research and innovation programme under grant agreement no.
634179 (EMPHASIS) (Effective Management of Pests and Harmful Alien
Species Integrated Solutions) and grant agreement no. 633999 (EUCLID)
(EU-CHINA Lever for IPM Demonstration).
The author(s) declare no conflict of interest.
Accepted for publication 8 May 2019.
© 2019 The American Phytopathological Society
and small, local firms. Fresh-cut products such as ready-to-eat salads
require substantial capital investment in plants and machinery. The
intensive nature of cultivation methods must be coupled with sus-
tainable practices. For example, the plastic films used for
manufacturing bags must permit specific respiration rates of the pro-
cessed vegetables inside the bag; investment in research and devel-
opment for new films is a continuous process (Mangaraj et al. 2009;
Ruiz-Cabello et al. 2015). Processes that maintain the cold chain
of bagged salad products is extremely important, since small devi-
ations from the ideal temperature can degrade product quality (Calvin
et al. 2006). In Europe, milk production facilities often also specialize
in ready-to-eat salads, since both products require daily delivery.
A Little History
The salad sector cannot be considered new at all. According to his-
torians, ancient Greeks and Romans consumed raw vegetables with
oil-based dressing. In particular, Romans taught Etrurians how to
use vegetables. In the recipe book written in the 1st century by Marco
Gavio Apicio (De re coquinaria), a full chapter is devoted to vegeta-
bles. Romans preferred strong flavors, including chicory as a salad
green for its bitter flavor and for its aid in digestion and sleep. Virgil
describes a rustic salad made of herbs, vinegar, and cheese, thus pre-
ceding the classical American Caesar salad (Pellati 2011) while Pli-
nium describes how convenient fresh vegetables are because they
require no cooking. The lettuce cultivar Romana (Romaine) seems
to belong to the old Romans and at least 12 types of lettuce were known
in ancient Rome. During the Middle Ages and the Renaissance,
Plant Disease / September 2019 2153
gardens for producing vegetables were very popular. Bartolomeo Sacchi produced in California and Arizona (Smith et al. 2011; USDA
(1493) described in details the many leafy vegetables and herbs grown 2017). U.S. sales of fresh-cuts grew from about $5 billion in 1994
and used in cooking (Pellati 2011). Vegetables are present in many to $10 to 12 billion in 2006, representing about 10% of total produce
still life paintings from the Renaissance. Nowadays, the increasing pop- sales to retailers and food service companies (Fouayzi et al. 2006). In
ularity of vegetarian and vegan eating habits contributes to add to the Japan and Korea, the fresh-cut produce market reached approxi-
popularity of salad crops all over the world. Indeed, ready-to-eat salads mately $2.6 billion in 2005 (Kim 2006). Ready-to-eat bagged lettuce
combine the advantages of convenience food and healthy eating. and prepared salads are a niche market in China, predominantly rep-
resented by the affluent younger generation of Chinese middle class
The Ready-to-Eat Salad Production and Market consumers in the largest cities (Gordon and Baroke 2016).
Interest in ready-to-eat salads is increasing worldwide and shows
enormous potential for further growth. Many new countries are join- Crops Grown, Features, and Cultivation Systems
ing those that traditionally have high consumption of fresh cut salad, Lettuce (Lactuca sativa L.), wild (Diplotaxis tenuifolia De Can-
attracted by their convenience and health benefits. Despite a long- dolle) and cultivated (Eruca sativa Mill.) rocket, lamb’s lettuce
term decrease in the consumption of fruits and vegetables, fresh-cut (Valerianella olitoria L.), chicory (Cichorium intybus L.), endive
products represent an opposing trend. Ready-to-eat salads are mostly (Cichorium endivia L.), basil (Ocimum basilicum L.), spinach (Spi-
chosen by relatively high-income, health-conscious consumers (Baselice nacia oleracea L.), and Swiss chard (Beta vulgaris subsp. vulgaris
et al. 2014; Brunner et al. 2010; Buckley et al. 2007; Cassady et al. L.) are the most important crops. In order to respond to consumers’
2007). Interest in environmental sustainability has improved con- request for novelty, the industry is investing in the introduction of new
sumer receptivity to ready-to-eat products with ecologically conscious crop species (e.g., different Asian salads belonging to Brassicaceae
labels (Sillani and Nassivera 2015). Moreover, the shift of a significant such as Mizuna, Kale, Tatsoi, Hakusai, and Shu-tsoi) and selection
portion of the world population toward vegetarian or vegan habits has
driven an increase in the consumption of fresh vegetables and fruit
(Eurispes 2016). In Europe, Italy ranks first in per capita consumption
of bagged fresh vegetables, followed by the U.K., Spain and France,
and Germany (0.6 kg/person/year) (Nomisma 2015; Nielsen 2016,
2018a, 2018b). Italy produced 110,000 tons of fresh-cut vegetables in
2015, with a value of €744 million (Casati and Baldi 2016). Of the total
value sold, lettuce comprised 75.4% followed by wild rocket (9.5%),
spinach (4.5%), and Swiss chard (1.3%) (Casati and Baldi 2016).
In the U.S., made-to-order salads have become a big business in
the booming fast-casual restaurant category. IFPA estimated that
the precut, prewashed, and packaged fruit and vegetable market is
one of the fastest growing food categories in U.S. supermarkets, from
$3.3 billion in 1994 to $11 billion in 2000 and $12 billion in 2007
(Cook 2014). Packaged salads are the second-fastest selling item
in U.S. stores (60.8%), with $3 billion in annual retail sales in
2013, followed by fresh-cut vegetables at $1.4 billion (Cook
2014). Among leafy vegetables, lettuce is the second most consumed
vegetable in the U.S., behind only potatoes, and is the most valuable,
with annual sales in 2017 nearing $1.5 billion (AG MRC 2018). The
vast majority—96%—of leafy vegetables used in salad mix are Fig. 2. Baby-leaf lettuce and wild rocket grown under multitunnel cultivation.

Fig. 1. Leafy vegetable types for the ready to eat sector.

2154 Plant Disease / Vol. 103 No. 9

of new varieties more adapted to the packaging process, with extended
shelf life, and more suitable to the market demand (Fig. 1).
Leafy vegetables share several common features, including the
presence of a high number of varieties, seed production in few coun-
tries, often in developing areas (Chile, China, Vietnam, Italy, Den-
mark, the Netherlands, and the U.S.A., mainly California and
Washington State), susceptibility to a number of pathogens and lim-
itations in the use of chemicals for their control (Gullino et al. 2014a),
coupled with general market requirements for long shelf life and zero
detectable pesticide residues. Leafy vegetables are generally grown
under protection (in most cases in plastic tunnels or greenhouses),
although some crops can also be grown in the open field.
In Italy, the area for the production of fresh-cut vegetables is about
6,500 ha, mainly in plastic tunnels (in northern Italy) or multitunnels
(in southern Italy) (Fig. 2) with five to six production cycles per year
(Casati and Baldi 2016).
In many countries, an increasing number of farms are adopting
soilless systems, since this cultivation method reduces soil contam-
ination by pesticide, uses less water, and produces more uniform
crops (Tomasi et al. 2015). Soilless cultivation permits direct control
of the nutrient solution, making it possible to modify composition
and concentration to achieve predictable results in relation to dry
matter content, nitrate content, or other organoleptic features of pro-
duce (Frezza et al. 2005). Lettuce is one of the most suitable crop for
soilless systems because it can be produced in a short period. Accord-
ing to Gonnella et al. (2003), floating cultivation produces acceptable
yield and good quality control parameters in baby leaf species
(shorter growing cycles, improved uniformity of growth, automation
of cultural techniques, and high levels of hygiene and quality).
Lamb’s lettuce, spinach, and Swiss chard are increasingly grown
in soilless systems (Petropoulos et al. 2016; Savvas and Gruda
2018). Water culture systems are predominantly used for production
LETTUCE TYPES
Types of lettuce for the ready-to-eat sector reflect the need
for more nutritious products and greater postharvest needs
(longer shelf life, for instance) as well as to innovation in
processing technology. There are four distinct types of
lettuce: leaf (also called loose-leaf lettuce), Romaine (syn.
Cos), crisphead (syn. Iceberg), and butterhead. Breeding
activities have provided innovative lettuce types, such as
the sortotypes ‘Izi Leaf’ (Eazy-Leaf) and ‘Salanova’ with an
elegant rosette of leaves, developed to produce the
minimum amount of waste at cutting and increased
postharvest storage.
Fig. 3. A, Discoloration caused by Fusarium oxysporum f. sp. lactucae on lettuce. B, Symptoms of Fusarium wilt on lettuce grown in an open field.
of leafy vegetables, such as lettuce (van Os 2017; van Os et al. 2008).
Hydroponic systems are commonly used in Spain, France, Belgium,
Germany, Italy, Japan, South Korea, Israel, Colombia, and China.
They are most popular in the Netherlands, with almost 95% of green-
houses being equipped with this method of production (Hickman
2011, 2017). In the United States, nearly all vegetables produced
in greenhouses are grown in hydroponic or soilless systems; about
1,425 ha of greenhouse are used to produce vegetables (tomatoes,
peppers, cucumbers, and lettuce), of which 16 ha are devoted to let-
tuce (Holmes 2017). Florida, with 155 ha in 2013, has seen a very
rapid increase in protected lettuce (Hochmuth and Toro 2014).
Worldwide, estimated greenhouse vegetable area is 489,214 ha,
while soilless/hydroponic systems for vegetables account for
95,000 ha (Hickman 2011, 2017). Leafy vegetables are also used as
a model for new cultivation methods such as vertical farming, which
involves stacking growth rooms such as glass-houses and controlled
environment rooms on top of each other to construct food-producing
high-rise buildings (Despommier 2011; Touliatos et al. 2016).
Why Have So Many New Diseases Developed?
Several factors are responsible for the development of many dis-
eases, often new ones, in this production sector. These seasonal prod-
ucts are grown under high crop density in five to six cycles per year in
the same substrate, in specialized farms, with a lack of adequate crop
rotation, and a shortage of fungicides labeled for their control. Interest
in the phytopathological problems of leafy vegetables grown for the
ready-to-eat salad sector is relatively recent, and a number of new dis-
eases have been reported (Table 1). Global travel and the international
trade of agricultural seeds and products have moved crops and patho-
gens away from their original environments. Most fungal diseases re-
cently described for leafy vegetables are seedborne (Gilardi et al.
2018a; Gullino et al. 2014a). Often, very low levels of seed contami-
nation can lead to the rapid emergence of new diseases in different geo-
graphic areas, with severe losses (Table 2). In this respect, downy
mildew of basil and Fusarium wilt of lettuce represent two very inter-
esting case studies (Farr and Rossman 2019). The arrival of a pathogen
in a new environment can disrupt its biological equilibrium and be re-
sponsible for the start of devastating epidemics. Climate change, gen-
erated by human activities, leading to an increase in greenhouse gases,
and resulting in an increase in temperature and shifts in rainfall pat-
terns, interacts with globalization to influence the development and
spread of plant pathogens (Anderson et al. 2004; Chakraborty and
Newton 2011). In this production sector, stringent quality control re-
quirements of the industry must be satisfied. For instance, a threshold
of damage to leaves is low—if more than 5% of leaves are affected, the
product is unmarketable. On the other hand, the high risk of economic
losses fosters careful monitoring of phytosanitary conditions and early
detection of diseases during crop production.
Plant Disease / September 2019 2155
Case Studies
Fusarium wilts. Fusarium wilts are among the most common dis-
eases on leafy vegetables and different formae speciales of Fusarium
oxysporum have been described on a number of leafy vegetable crops
(Gilardi et al. 2018a; Matheron and Gullino 2012).
In recent years, Fusarium wilt has become the most important dis-
ease of lettuce in all cultivation areas throughout the world. Its spread
is favored by seed transmission (Cabral et al. 2018; Garibaldi et al.
2004a). Until very recently, three races of F. oxysporum f. sp. lactu-
cae had been described (Fig. 3A and B): race 1 is the most wide-
spread in Europe, the U.S.A., and South America (Matheron and
Gullino 2012), and races 2 and 3 in Taiwan and Japan (Fujinaga
et al. 2001, 2003, 2005). In 2017, race 4 was detected in the Nether-
lands (Gilardi et al. 2017a). This new race is rapidly spreading and
has been reported to date in Belgium (Claerbout et al. 2018), the
U.K., and Ireland (Taylor et al. 2019), posing serious threats to
growers and breeders. Until resistant varieties are developed, preven-
tive management measures, such as the use of healthy seeds and/or
seed treatments, are required to reduce the risk of its spread to new
cultivation areas.
A careful monitoring of F. oxysporum f. sp. lactucae race situation
in the field is useful for deployment of resistant cultivars (Fig. 4). The
use of specific molecular markers can help to satisfy this goal by en-
abling detection and identification of formae speciales and races of F.
oxysporum from seeds, plants, and soil samples (Franco-Ortega et al.
2018; Pasquali et al. 2008).
Three vegetative compatibility groups (VCGs), VCG-300, VCG-
301, and VCG-302, corresponding to races 1, 2, and 3, respectively,
have been reported in the forma specialis lactucae (Fujinaga et al.
Fig. 4. Screening with differential cultivars of lettuce for evaluation of races of
Fusarium oxysporum f. sp. lactucae.
Fig. 5. Symptoms of Fusarium wilt on wild rocket.
2156 Plant Disease / Vol. 103 No. 9
2005; Ogiso et al. 2002; Pasquali et al. 2005; Pintore et al. 2017;
Yamauchi et al. 2004). The Italian isolates (Garibaldi et al.
2004b), the Arizona, California, and Japanese isolates and type 2 iso-
lates from Taiwan (Huang and Lo 1998) all belong to the same VCG
0300 defined for race 1 (Mbofung et al. 2007; Pasquali et al. 2005),
suggesting the spread of a common clone in different countries, prob-
ably by propagation material. In addition, the sequence-specific am-
plified polymorphism (SSAP) technique confirmed the worldwide
clonality of VCG 0300 race 1 (Pasquali et al. 2008). Moreover, all
race 1 isolates from Arizona, California, and Japan have identical
mtSSU and EF-1a sequences and almost identical intergenic spacer
(IGS) region sequences, which would seem to suggest a common or-
igin, and the race 2 isolate from Japan and the type 1 isolates from
Taiwan grouped together (Pasquali et al. 2007). Isolates of F. lactu-
cae race 4 from lettuce in the Netherlands belong to VCG-303
(Pintore et al. 2017). Further studies are needed to elucidate how
the new race has developed in Europe.
Fusarium wilts have also been observed on wild and cultivated
rocket (Fig. 5), lamb’s lettuce (Fig. 6), chicory, endive, basil, and
spinach, with severe losses on all crops. Wilt of Eruca sativa
and Diplotaxis spp. is attributed to F. oxysporum ff. spp. raphani
and conglutinans, with the first forma specialis being the most fre-
quently detected. It also affects other genera belonging to Brassica-
ceae, such as cabbage, Brussel sprouts, broccoli, turnip, and radish
(Garibaldi et al. 2006a) and Valerianaceae such as lamb’s lettuce
(Srinivasan et al. 2010). F. oxysporum f. sp. spinaciae is also a seri-
ous constraint to spinach and beet production worldwide (Correll et al.
1994; Larsson and Gerhardson 1992). One common feature of the causal
Fig. 6. Symptoms of Fusarium wilt on lamb’s lettuce.
Fig. 7. Severe losses caused by Pythium damping-off on wild rocket.
agents of Fusarium wilt is the fact that they can be carried by seeds, as
shown in the case of F. oxysporum f. sp. lactucae on lettuce (Garibaldi
et al. 2004a), F. oxysporum f. sp. conglutinans and F. oxysporum f. sp.
raphani on wild and cultivated rocket (Garibaldi et al. 2004c) and spin-
ach (Bassi and Goode 1978; Correll et al. 1994), and F. oxysporum f. sp.
basilici on basil (Martini and Gullino 1991).
Pythium damping-off. Among the soilborne diseases, damping
off, caused by Pythium ultimum, has been increasingly observed on let-
tuce, wild rocket, and lamb’s lettuce at temperatures between 15 and
25°C. The presence of newly recorded species of Pythium (Matić
et al. 2019a), such as P. aphanidermatum on spinach (Garibaldi et al.
2015b) and swiss chard, P. irregulare on lamb’s lettuce (Garibaldi
et al. 2015a), Pythium Cluster B2a on lettuce (P. dissotocum, P. colora-
tum, P. diclinum, P. cf. dictyosporum, P. lutarium, P. sp. ‘Group F’, and
P. sp. tumidum) (Garibaldi et al. 2017a), and P. sylvaticum on lettuce
(Gilardi et al. 2018c), is particularly evident at warm temperatures
and may become highly destructive in monoculture (Fig. 7).
Other soilborne pathogens. In part because of their wide host
range, Sclerotinia species (S. minor and S. sclerotiorum) (Fig. 8)
and Rhizoctonia solani cause serious losses in most production areas
(Garibaldi et al. 2005b, 2006b; Nicoletti et al. 2004; Subbarao et al.
2017). Generally, attacks on lettuce, rocket, lamb’s lettuce, spinach,
and Swiss chard grown at high density develop as circular areas of
infected plants (Fig. 9A and B). In addition, Thielaviopsis basicola
may cause extensive damage, as reported on lettuce in California
and Australia (Subbarao et al. 2017) and on lamb’s lettuce in Italy
(Garibaldi et al. 2005a).
Fig. 8. Attacks of Sclerotinia sclerotiorum on wild rocket.
Fig. 9. A, Attacks of Rhizoctonia solani on lettuce grown under a plastic tunnel. B, Close up of symptoms caused by R. solani on lettuce.
Leaf Spots
Some of the newly introduced pathogens that are typical of warm
areas are spreading into temperate regions due to the increase in air
temperature. Given the predicted increase in global air temperatures
and CO2 concentrations, downy mildew on basil, Alternaria leaf spot
on rocket, Phoma leaf spot on swiss chard and lettuce, Myrothecium
leaf spot on spinach, and Fusarium equiseti leaf spot on wild rocket
and lettuce are expected to become more problematic (Chitarra
et al. 2015; Gilardi et al. 2016b; Gullino et al. 2017a, 2017b, 2018;
Siciliano et al. 2017a, 2017b). In this section, some recently reported
foliar diseases are described.
Plectosphaerella cucumerina. This filamentous ascomycete is
cosmopolitan in distribution, and has been reported on many hosts
such as melon, watermelon, squash, courgette, cucumber, basil, to-
mato, sunflower, white lupin, parsley, and banana (Carlucci et al.
2012; Matta and Garibaldi 1981; Farr and Rossman 2019; Palm
et al. 1995; Pétriacq et al. 2016) causing a wide range of symptoms,
including crown and root rot as well as leaf necrosis. This species,
which can change from hemibiotrophic to necrotrophic (Pétriacq
et al. 2016), has been observed on lamb’s lettuce (Carrieri et al.
2014), wild rocket (Fig. 10), and endive (Gilardi et al. 2018a), asso-
ciated with severe losses. The affected leaves show spots on the leaf
blade, rib, and petiole that are usually surrounded by yellow-gray hal-
oes. Damaged tissues rot quickly after packaging, but also during
transit and commercialization. Rapid spread of the disease that oc-
curred in Italy on wild rocket in 2012 has been explained by the ca-
pability of the pathogen to infect seeds (Gullino et al. 2014a). P.
cucumerina is a nematophagous fungus that had previously been
considered as a potential biological control agent (Atkins et al.
2003). Its ability to survive as a saprotroph in soil (Domsch and
Gams 1972), its polyphagous nature, and its capability to contami-
nate seeds makes its management difficult.
Alternaria leaf spot. Species of Alternaria are threats to several
leafy vegetables in many production areas. Sweet basil was found to
be a new host for Alternaria sp. in California, Florida, Pakistan, Ja-
pan, and Israel (Farr and Rossman 2019; Kenigsbuch et al. 2010;
Taba et al. 2009). Since 2010, A. alternata has been found to cause
a leaf spot disease on sweet basil plants grown in soil-less systems, as
well as on the most popular variety grown for fresh consumption and
pesto production in soil (Gullino et al. 2014a). This pathogen has
been isolated at high incidence (from 7.3% and 2.6% on nondisin-
fected and disinfected seeds, respectively) from several commercial
seed lots, suggesting an important role of seeds in pathogen dissem-
ination (Gilardi et al. 2013b).
Alternaria japonica has consistently been isolated from wild and
cultivated rocket plants (Fig. 11) (Gilardi et al. 2018a), affecting
yield and quality of hydroponically grown cultivated rocket (Tidwell
et al. 2014). Wild and cultivated rocket seeds may be responsible for
Plant Disease / September 2019 2157
disseminating the pathogen because of their external contamination
(Gilardi et al. 2015b). Alternaria tenuissima, A. brassicicola, and A.
arborescens have also been detected on wild and cultivated rocket
plants and seeds, which suggests that these species are also potential
threats to rocket, although A. japonica has been found to be the most
prevalent species (Siciliano et al. 2017c). A. spinaciae and A. alter-
nata have been found on spinach (Farr and Rossman 2019).
The different species of Alternaria, once introduced into the field,
can survive on plant debris, with a high potential to cause severe los-
ses on a large number of leafy vegetables grown in succession. Fur-
thermore, Alternaria spp. are potential producers of mycotoxins,
such as tenuazonic acid, alternariol, alternariol monomethyl ether,
altenuene, and tentoxin, and as a result should be considered a threat
to humans (Ostry 2008).
Fusarium equiseti. This seedborne pathogen generally occurs in
tropical and subtropical regions on a wide range of plants (including
cotton, lentil, sugar beet, cumin, potato, cowpea, pine, ginseng, and
asparagus) on which it causes a variety of symptoms (Farr and Rossman
2019). In 2010, cultivated and wild rocket (Fig. 12) and lettuce were
found as new hosts of F. equiseti (Gilardi et al. 2018a). The same
pathogen has recently been reported on radish (Raphanus sativus
L.) seedlings in a nursery (Garibaldi et al. 2017b), with yield losses
of about 10% at temperatures of between 15 and 30°C and under high
relative humidity. Lettuce and rocket are particularly susceptible to
F. equiseti at temperatures from 25 to 35°C; at these temperatures,
short periods of high relative humidity are sufficient to reduce yield
Fig. 10. Plectosphaerella leaf spot on wild rocket.
Fig. 11. Leaf spot caused by Alternaria japonica on cultivated rocket.
2158 Plant Disease / Vol. 103 No. 9
and quality (Gullino et al. 2017a). F. equiseti has been found as an
external seed contaminant on Diplotaxis spp. (Gilardi et al. 2017c),
which suggests that seeds may be important in its spread throughout
several production areas. Once introduced, it survives as a saprotroph
in soil or crop debris, and is thus very adaptable to different cropping
systems, particularly intensive ones. The broad host range of F. equi-
seti, together with its ability to produce a diversity of mycotoxins,
including trichothecenes and fumonisins, causes further health risks
(Bosch and Mirocha 1992; Bottalico 1988; Desjardins 2006).
Myrothecium leaf spot. The genera Paramyrothecium and Albi-
fimbria were recently established from the ex-genus Myrothecium,
comprising common soil-inhabiting and saprophytic fungi. They
are causal agents of leaf spots and stem rot on about 20 different plant
species, including cotton, tomato, cacao, coffee, potato, soybean, cu-
curbits, maize, and many ornamentals (Farr and Rossman 2019), and
are in many cases seed-transmitted (Belisario et al. 1999; Bharath
et al. 2006). Only two species are known to be phytopathogenic; Par-
amyrothecium roridum and Albifimbria verrucaria cause a necrotic
leaf spot and plant dieback, respectively.
Severe leaf necrosis and plant decay caused by P. roridum were re-
cently observed on lamb’s lettuce, while A. verrucaria has been iso-
lated from spinach and wild rocket (Fig. 13A, B, and C) (Gilardi
et al. 2018a; Matić et al. 2019b). A characteristic that makes this spe-
cies a serious threat to the productivity of spinach and wild rocket is its
capacity to produce macrocyclic trichothecenes, which are dangerous
cytotoxic compounds (Bosio et al. 2017; Siciliano et al. 2017b).
Other leaf spots. Additionally, species in the genus Phoma on let-
tuce (Allophoma tropica) (Fig. 14), lambs’ lettuce (Phoma valeria-
nellae), Swiss chard (P. betae) and Stemphylium (S. botryosum
and S. beticola) on spinach represent a potential threat to leafy veg-
etables in several production areas (Farr and Rossman 2019; Gilardi
et al. 2018a, 2018b). A different species, Boeremia exigua (syn. P.
exigua), was first reported to cause leaf spot and basal rot on lettuce
in the United Kingdom, and on field grown lettuce in California
Fig. 12. Leaf spot caused by Fusarium equiseti on wild rocket.
(Subbarao et al. 2017).The symptoms caused by these pathogens are
very similar, and often vary depending on the age and nutritional sta-
tus of the plants. Symptoms can also be confused with those caused
by other pathogens such as Botrytis cinerea.
Trends in Disease Management
Ready-to-eat salads must be appealing, without visible damage to
the leaves and must pass stringent quality standards. The manage-
ment of the many traditional and emerging diseases of leafy vegeta-
bles grown for ready-to-eat salads represents a real challenge.
Importantly, except for lettuce, there are few fungicides or bacteri-
cides registered for use on these crops. Therefore, non-pesticide al-
ternatives are needed. For instance, in hydroponic crops, potassium
silicate, supplied via nutrient solution at 100 mg liter−1, reduced
downy mildew severity on lettuce by 33 to 78%, and improved crop
quality when grown under highly saline conditions (Garibaldi et al.
2012). Silicates were also effective against A. japonica on rocket,
Colletotrichum gloeosporioides on basil, and Bremia lactucae on let-
tuce grown in soilless systems (Table 3) (Gullino et al. 2015),
while potassium silicate and the increased electrical conductivity im-
proved Fusarium wilt control on lettuce by up to 50% (Chitarra et al.
2013).
Seed health. A primary preventive strategy is the use of healthy
seeds. Stock seeds should be produced in regions associated with
the lowest possible disease risk, and should be subjected to
Fig. 13. A, Myrothecium leaf spot on lamb’s lettuce. B, Myrothecium leaf spot on spinach. C, Myrothecium leaf spot on wild rocket.
HUMAN PATHOGENS
Leafy vegetables can be infested, if hygienic conditions are
not fully respected, by food-borne pathogens such as
Escherichia coli, Salmonella enterica, and Listeria
monocytogenes (Brandl 2006). Ready-to-eat products go
through intensive control programs, according to national
and international regulations, which define the presence and
microbiological limits for E. coli, including some
verocytotoxigenic E. coli, L. monocytogenes, and
Salmonella spp. Despite these rules, human pathogens on
ready-to-eat products have been detected worldwide
(Francis et al. 1999; Jeddi et al. 2014; Kovačević et al. 2013;
Legnani and Leoni 2004; Losio et al. 2015; Söderqvist 2017).
Some are not plant pathogens but rather use plants as
vectors to humans (Barak and Schroeder 2012). Outbreaks
of hemorrhagic strains of E. coli O157-H7 and Salmonella
sp. on edible crops in many countries attracted the attention
of plant pathologists (Fletcher et al. 2013). In general, enteric
bacterial pathogens enter agricultural environments via
animal feces. Crops can be contaminated through water,
soil, compost, and seed (Barak and Schroeder 2012). Strict
cultural controls, including the use of sanitizers, combined
with monitoring done by regulatory agencies, help to avoid
contamination by food-borne pathogens.
Plant Disease / September 2019 2159
standardized seed health analysis (Munkvold 2009). The availability Verticillium, and Alternaria spp. by 88, 74, and 84%, respectively,
of sensitive, reliable diagnostic tools for early pathogen detection but it was not effective against F. oxysporum. Thyme and savory es-
represent the best preventative options in many cases (Thomas sential oils, applied by spraying lettuce seeds at 1%, provided 77 and
et al. 2017), as has been observed for P. cucumerina on wild rocket 78% reductions of Fusarium wilt, respectively (Gullino et al. 2014b).
(Gilardi et al. 2016d) and formae speciales and races of F. oxysporum Biocontrol agents (Bacillus subtilis MBI 600, B. subtilis QST 713,
from seeds, plants, and soil samples (Gilardi et al. 2017a; Mbofung Streptomyces griseoviridis K61, Pseudomonas fluorescens L 18, Tri-
and Pryor 2010; Pasquali et al. 2007). choderma viride TV6903) and thyme oil were as effective as thiram,
Rapid and reliable detection methods are also essential to identify resulting in 40 to 75% efficacy against A. brassicicola on brassica
the causal agents of the different diseases in the field, helping exten- seeds (Amein et al. 2011). Among physical treatments, aerated steam
sion services and growers to adopt preventative control measures. (Forsberg et al. 2005) was effective (70% of healthy plants), while
Loop-mediated-isothermal amplification (LAMP) methods can be the electron seed treatment, based on the biocidal effect of low-en-
used to diagnose pathogenic agents in the field. A LAMP protocol ergy electrons (Jahn et al. 2005) was most effective when combined
was recently developed for the rapid detection of F. oxysporum with thyme oil (80% of healthy plants) against A. brassicicola
f.sp. lactucae from lettuce seeds, soil, and plant material (Franco- (Amein et al. 2011).
Ortega et al. 2018) and for Pythium irregulare, P. uncinulatum, Nonchemical seed treatments such as dry heated air (65°C for
and P. spinosum in lettuce production (Feng et al. 2019). 10 min), resistance inducers, and thyme oil seed treatments are effec-
In order to reduce the risk posed by seed-borne pathogens, it is rec- tive against basil downy mildew, although the protection offered
ommended that stock seeds undergo precautionary decontamination varies between 37 to 78%, according to the level of seed infection
treatments. Chemical seed treatments are used for a wide range of
crops against different seed-borne pathogens (Koch and Roberts
2014; Munkvold 2009). Treatments with hot water, aerated steam,
or dry heat can be very effective, but need to be optimized due to
the differences in temperature and time required for different target Table 1. Main foliar and soil-borne pathogens detected in Italy on
leafy vegetables grown for the ready-to-eat sector (updated from
pathogens and hosts (McGrath 2013; Nega et al. 2003). The main Gullino et al. 2014a)
disadvantage of treating seeds with hot water is the need for post-
treatment drying (Koch and Roberts 2014). For instance, hot water Year of
seed treatments of 40°C for 10 min reduces or eliminates Cladospo- Host Species Pathogen detection
rium variabile on spinach seeds without damaging germination, Cultivated Eruca Alternaria japonica 2010
whereas 55 or 60°C for $10 min are necessary against Stemphylium rocket vesicaria
botryosum, with partial results in highly infected seed lots (du Toit Fusarium oxysporum 2003
and Hernandez-Perez 2005). A technology based on aerated steam f. sp raphani
is now in commercial use for the treatment of cereal and vegetables Fusarium equiseti 2011
Colletotrichum kahawae 2014
seeds in The Netherlands, Sweden, and Norway, with more accurate Wild rocket Diplotaxis Fusarium oxysporum 2003
control of temperature and humidity that leaves seeds much dryer and tenuifolia f. sp raphani
reduces impact on seed germination (Fosberg et al. 2005; Koch and Rhizoctonia solani 2004
Roberts 2014). Alternaria japonica 2010
Although nonchemical seed treatments, including resistance in- Plectosphaerella 2012
ducers, antagonistic microorganisms, and fungal and plant extracts, cucumerina
are being investigated intensively, especially for seeds produced un- Fusarium equiseti 2014
Albifimbria verrucaria 2015
der organic farming rules, there are only a few examples of their com- Lettuce Lactuca Fusarium oxysporum 2002
mercial use (Gullino et al. 2014b; Koch and Roberts 2014). sativa f. sp. lactucae
Pseudomonas spp. and nonpathogenic strains of F. oxysporum Allophoma tropica 2011
251/2 and MSA35, and a commercial formulation of Trichoderma Fusarium equiseti 2014
gamsii plus T. asperellum applied as wet or dry powder on lettuce Pythium Cluster B2a 2015
seeds artificially infested with F. oxysporum f.sp. lactucae, reduced (P. dissotocum,
the pathogen on the surface of the seed but did not control internal P. coloratum, P. diclinum,
P. cf. dictyosporum,
infection (Table 4) (Lopez-Reyes et al. 2014). Among several micro-
P. lutarium, P. sp.
organisms tested by Cummings et al. (2009), Streptomyces griseovir- ‘Group F’ and P. sp.
idis reduced contamination of spinach seeds by S. botryosum, tumidum)
Pythium sylvaticum 2015
Lamb’s Valerianella Fusarium oxysporum 2004
lettuce olitoria ff. spp. raphani and
conglutinans
Rhizoctonia solani 2004
Pythium irregulare 2013
Phoma valerianellae 1966
Plectosphaerella cucumerina 2014
Paramyrothecium roridum 2015
Basil Ocimum Fusarium oxysporum 1989
basilicum f. sp. basilici
Peronospora belbahrii 2003
Alternaria alternata 2010
Swiss Beta vulgaris Pleospora betae 2007
chard subsp. Pythium aphanidermatum 2010
vulgaris
Spinach Spinacia Fusarium oxysporum 2011
oleracea f. sp. spinaciae
Pythium aphanidermatum 2014
Albifimbria verrucaria 2015
Stemphylium beticola 2017
Alternaria alternata 2017
Fig. 14. Leaf spot caused by Allophoma tropica on lettuce.

2160 Plant Disease / Vol. 103 No. 9

(Gilardi et al. 2015c; Lopez-Reyes et al. 2014, 2016). In view of a plant material treated to preserve isothiocyanate activity. The appli-
fully IPM approach, dry heated air (65°C for 10 min) treatment of cation of B. carinata (as pellet and flour) and compost 30 days before
basil seeds combined with foliar sprays with a tank mixture of planting showed up to 50% control of Fusarium wilt of lettuce
azoxystrobin or mandipropamid with potassium phosphite, re- (Gilardi et a. 2016c). However, a possible negative effect of the
duced severity of P. belbahrii by 95% (Gilardi et al., personal use of Brassica pellets due to an increase of pathogen inoculum po-
communication). tential has been observed. Brassica pellets can serve as a substrate
Soil health. Strict limits on fumigations due to regulatory restric- sustaining saprophytic growth of pathogens such as Pythium (Mazzola
tions complicate management of soilborne pathogens. The few fumi- et al. 2012), and brassicas used as intercrops are susceptible hosts of
gants that are still available should be applied accordingly to the Fusarium wilt pathogen of rocket (Lu et al. 2010).
sustainable use rules (Colla et al. 2014). In a field experiment, for Genetic control. Use of resistant cultivars is potentially the most
example, dimethyl disulphide (DMDS), applied at preplanting as a effective choice to control lettuce Fusarium wilt (Gordon and Koike
shank injection, alone or in combination with metham sodium, sig- 2015; Matheron and Gullino 2012). A possible association between
nificantly reduced Fusarium wilt of lettuce (from 70 to 100% when horticultural type and resistance to Sclerotinia has been observed for
used at the highest rate of 60 g/m2), with positive effects on yield and lettuce, with the highest levels of resistance showed by stem or
weed control. Dazomet can also provide noticeable reduction (40.5 to
74.3% when used at 50 g/m2) of Fusarium wilt of lettuce (Gilardi
et al. 2017b).
Although in the past the management of soilborne pathogens was
mostly based on soil disinfestation treatments that were able to limit Table 3. Effect of potassium silicate and increased concentration of
diseases and losses from a number of pathogens and pests, more spe- electrical conductivity (EC) of the nutrient solution on disease
cific treatments are now being carried out against the most relevant severity of different leaf spots on leafy vegetable crops grown in
problems (Garibaldi et al. 2014; Katan 2017). Like other soilborne soilless systems. Data are expressed as percentage of affected leaf
pathogens, Fusarium wilt is difficult to manage with a single ap- area at the end of the trials (from Gullino et al. 2015).
proach and/or with a single product, so integrated strategies are Alternaria
needed (Gordon and Koike 2015; Katan et al. 2012; Matheron and Bremia japonica on Colletotrichum
Gullino 2012). K silicate EC lactucae cultivated gloeosporioides
Applying organic matter (compost, animal manure, vegetable crop (100 mg/liter)y (mS/cm) on lettuce rocket on basil
residues, and organic amendments) to the soil improves disease sup-
No 1.8–2.0 15.6 ez 8.2 d 23.2 c
pression against different soilborne pathogens, with a variable degree Yes 1.8–2.0 13.7 de 6.5 cd 17.3 b
of success (Bonanomi et al. 2010). Despite the important role of or- No 2.5–3.5 10.5 cd 5.8 c 6.6 a
ganic amendments in maintaining plant health within an IPM frame- Yes 2.5–3.5 6.8 bc 3.6 b 5.7 a
work, there are concerns about food safety risks associated with the No 4.0–4.2 2.6 ab 2.6 ab 5.8 a
use of animal manure and compost, related to potential microbial and Yes 4.0–4.2 1.3 a 0.9 a 4.4 a
chemical contamination and internalization of some strains of human y
K silicate applied at 100 mg/liter.
z
pathogens on lettuce plants (Chitarra et al. 2014). Biofumigation in The mean values of the same column followed by the same letter do
the case of intensive agricultural systems can also be achieved by in- not differ significantly according to Tukey test (P = 0.05).
corporating seed meals (i.e., Brassica carinata seed meal) or dried

Table 2. Contamination of seeds of lettuce, endive, chicory, rocket, corn salad, spinach, and basil by different pathogens (updated from Gullino et al.
2014a)
Crop Pathogen % of infected seeds Reference
Lettuce Fusarium oxysporum f. sp. lactucae 0.1 Garibaldi et al. 2004a
Verticillium dahliae 66–90 Vallad et al. 2005
Botrytis cinerea 30 Sowley et al. 2010
Microdochium panattonianum -z Sutton and Holderness 1986
Endive, chicory, Alternaria cichorii 0.6–13.75 Barreto et al. 2008.
escarole
Rocket Fusarium oxysporum 0.1 Garibaldi et al. 2004c
Plectosphaerella cucumerina 0.15 Gilardi et al. 2013a
Alternaria japonica 0.4 (external contamination) 0.2 (embrio Gilardi et al. 2015b
contamination)
Fusarium equiseti 0.1–0.6 (external contamination) Gilardi et al. 2017c
Lamb’s lettuce Phoma valerianellae 0.6–15 Pellegrino et al. 2010
Acidovorax valerianellae 5.6–20.5% Thiele et al. 2012
Spinach Fusarium oxysporum f. sp. spinaciae - Bassi and Goode 1978
Peronospora farinosa f. sp. spinaciae races 1, 0.3–2.9 Lorenzini and Nali 1994;
2, 3, 4 Inaba et al. 1983
Cladosporium variabile 1.8 Matta and Garibaldi, 1981;
Hernandez-Perez and du Toit 2006
Stemphylium botryosum 1–95 Hernandez-Perez and du Toit 2006
Verticillium dahliae 0.3–84.8 du Toit et al. 2005
Basil Fusarium oxysporum f. sp. basilici 0.4 (external contamination) 0.2 (embrio Martini and Gullino 1991
contamination)
Peronospora belbahrii 0.01 Garibaldi et al. 2004d
Alternaria alternata 0.2–15.0 (external contamination) 0.2–2.0 Gilardi et al. 2013b
(embrio contamination)
Albifimbria verrucaria - Matić et al. 2019b
z
Data not available.

Plant Disease / September 2019 2161

romaine-type with upright growth habits and early bolting (Grube
and Ryder 2004).
Careful monitoring of the race situation in the field is also neces-
sary for an efficient use of genetic control approaches. For instance,
resistance genes can be overcome by new virulent phenotypes of dif-
ferent pathogens. This is the case for several cultivated lettuce culti-
vars belonging to the Batavian and Romaine type that are resistant or
at least tolerant to race 1 of F. oxysporum f. sp. lactucae (Garibaldi
et al. 2004b; Gilardi et al. 2014; Matheron and Gullino 2012; Scott
et al. 2010a, 2010b, 2014). However, their use in practice is compli-
cated by the presence of new races of these pathogens (Fig. 15)
(Gilardi et al. 2014). In the case of rocket, despite intensive research
that has been conducted to select resistant cultivars against Fusarium
wilt causal agents, it is difficult to adopt this strategy mainly due to
high variability in virulence of pathogen isolates (Fig. 16) (Gilardi
et al. 2007, 2014).
Resistance against downy mildew of lettuce and spinach is very
effective, and widely used by growers (Correll et al. 2011; Subbarao
et al. 2017). Unfortunately, resistance genes are recurrently over-
come by new virulent phenotypes of the causal agent (Feng et al.
2014; Lebeda et al. 2014).
Resistant cultivars against Pythium spp. and R. solani are generally
not available for most leafy vegetables.
Chemical control. In conventional head lettuce crops in the Med-
iterranean region, eight to 10 pesticides are applied on average to
manage pests and pathogens during the 60- to 90-day crop cycle
(Barrière et al. 2015). Regulatory restrictions limit growers to a small
number of different pesticide chemistries, resulting in repeated use of
the same active ingredients and consequently a high risk of resistance
development in some pathogen populations.
Due to the lack of host resistance, the management of some emerg-
ing pathogens on lettuce, such as A. tropica, is largely dependent on
fungicide treatment and cultural practices. For instance, fludioxonil,
iprodione, boscalid, and pyraclostrobin were found to be the most ef-
fective fungicides (up to 90% disease severity reduction) on lettuce
against A. tropica (Pintore et al. 2018). Efficacy shown against
A. tropica by fungicides that are effective against other important fo-
liar pathogens of lettuce help simplify the management of this emerg-
ing disease. For instance, a mixture of pyraclostrobin and boscalid is
one of the most widely used commercial formulations to control B.
cinerea and S. sclerotiorum on leafy vegetables in field and green-
house production (Leyronas et al. 2011; Matheron and Porchas
2004). In the case of foliar diseases, the few fungicides registered
for use on minor crops should be used in a limited number of sprays
to reduce the risk of residue level exceeding the legal values as well
as to avoid the selection of resistance to site-specific fungicides.
Resistance inducers and biocontrol agents. Among mineral sub-
stances, inorganic salts with biocidal effects have shown interesting
efficacy for the control of plant diseases, including leafy vegetables
(Deliopoulos et al. 2010). These substances can have a direct effect
on pathogens or can act as resistance inducers. Phosphite-based prod-
ucts tested against Plectosphaerella leaf spot on wild rocket were as
effective as acibenzolar-S-methyl, mandipropamid, and azoxystro-
bin, providing strong though not complete (from 55 to 81%) control
(Gilardi et al. 2015a). Terpenic copper and Streptomyces griseovir-
idis, which are products permitted in organic farming, provided a
positive effect (from 53 to 69%) in reducing the leaf spot by P. cucu-
merina on rocket (Gilardi et al. 2015a). An integrated approach is
necessary, considering the difficulty of reaching complete control
of this pathogen with single control measures.
Preventive treatments in nurseries facilitate more efficient use of
biocontrol agents. For instance, Bacillus subtilis QST713 reduces
Fusarium wilts in lettuce and rocket by up to 50% when applied start-
ing from the nursery, using three to four treatments in a short interval
(Table 5) (Gilardi et al. 2016a, 2019). However, biocontrol agents are
difficult to apply in this sector because they may affect the total mi-
crobial population over the leaf tissues with consequent problems for
shelf life and processing (Ragaert et al. 2007).
Conclusions
The phytosanitary situation of leafy vegetables grown for ready-
to-eat products is quite complex, with a large number and variety

Table 4. Efficacy of different products applied as powder and spray seed treatments of artificially inoculated lettuce seeds with Fusarium oxysporum f. sp.
lactucae, race 1. Data are average of four trials expressed as efficacy compared with the inoculated and nontreated control 40 days after sowing (from
Lopez-Reyes et al. 2014).
Treatment Dosage a.i./kg of seeds Seed application % of disease reduction
Inoculated and nontreated control - - 0.0 (27.7)x cy
Acibenzolar-S-methyl 0.1 g spray 59.2 ab
Prochloraz 1.0 g spray 91.6 a
Thiram 9.8 g spray 71.8 ab
Bacillus subtilis - QST 713 10.0 g spray 55.9 ab
Bacillus subtilis BA41; Streptomyces sp. SB15; Trichoderma 2.0 g mixing of dry powder 59.2 ab
harzianum TH02; Pseudomonas proradix 10; Glomus
caledonium GM24; Glomus coronatum GU53; Gladius
intraradices GB67; Trichoderma spp.
Streptomyces griseoviridis K61 8.0 g spray 35.3 b
Streptomyces spp. SB14; Glomus coronatum GO01; 2.0 g spray 40.7 b
Glomuscoronatum GU53; Glomus caledonium GM24; Bacillus
subtilis SR63; Pseudomonas spp. PM46; Ulocladium spp.
UO18
Trichoderma harzianum ICC 012 + Trichoderma viride ICC 080 2.0 g spray 66.1 ab
Glomus spp. 5% + Bacillus megaterium 104 CFUg−1 + 2.0 g spray 59.2 ab
Trichoderma 1010 CFUg–1
Pseudomonas sp. FC6B (EU836173) 1 × 107 CFUz spray 57.8 ab
Pseudomonas putida FC7B (EU836174) 1 × 107 CFU spray 69.7 ab
Pseudomonas sp. FC8B (EU836171) 1 × 107 CFU spray 66.1 ab
Pseudomonas sp. FC9B (EU836172) 1 × 107 CFU pray 76.1 ab
Pseudomonas sp. FC24B (EU836173) 1 × 107 CFU spray 53.8 ab
Fusarium oxysporum 251/2 1 × 107 CFU mixing of talc formulation 61.7 ab
Fusarium oxysporum MSA35 1 × 107 CFU mixing of talc formulation 52.3 ab
x
% of contaminated seeds in the inoculated nontreated control. Seed sample was naturally contaminated by Fusarium oxysporum f. sp. lactucae at 1.1%.
y
The mean values of the same column followed by the same letter do not differ significantly according to Duncan test (P = 0.05).
z
CFU = colony forming units.

2162 Plant Disease / Vol. 103 No. 9

of diseases causing severe losses. Disease pressure could worsen in
the future as a consequence of global warming. Indeed, many of the
pathogens recently detected are characterized by a preference for
high temperatures. Studies carried out under controlled environmental
facilities, which simulate future scenarios with higher temperatures and
CO2 values, evaluated several pathogens on leafy vegetables (Table 6)
(Gullino et al. 2018). Pathogens such as F. equiseti, Alternaria spp.,
Paramyrothecium, and Albifimbria are favored by such changes
(Gullino et al. 2018). The increase in temperatures predicted for the
future could also induce an upsurge of Fusarium wilts through
plant-mediated effects (Chitarra et al. 2015; Ferrocino et al. 2013).
In particular, climate change is likely to have direct influence on the
spatial and temporal dispersal of propagules, on the rapidity of disease
development, and on the pathogen survival or indirectly affect both the
host and the pathogen by changing, for example, the frequency of oc-
currence of suitable infection conditions (West et al. 2012).
In some cases, mycotoxin production could also be influenced by cli-
mate change (Table 7) (Gullino et al. 2018). Alternaria toxins are pro-
duced from 14 to 26°C, with significant differences according to the
host plants and strain used (Siciliano et al. 2017a). Tenuazoic acid is
the most frequently produced mycotoxin by Alternaria spp. under in-
creased temperature and higher carbon dioxide (Siciliano et al. 2017a).
While a significant variability in aggressiveness of Alternaria spp. from
brassica plants has been documented for different brassica hosts (Rotem
1994; Saharan et al. 2016), temperatures from 22 to 26°C and 800 ppm of
carbon dioxide generally caused an increase in leaf spot severity on rocket,
cauliflower, and cabbage (Siciliano et al. 2017a). An opposite trend of
mycotoxin production to that of virulence has been observed on rocket
and cauliflower grown under these conditions (Siciliano et al. 2017a).
The severity of leaf spot caused by F. equiseti on rocket and radish
was found to increase at 850 ppm of carbon dioxide at temperatures
of between 22 and 30°C, thus providing further support to the

Fig. 15. Susceptibility of several lettuce cultivars used in the ready-to-eat sectors in Italy artificially inoculated with the Italian (Race 1) and Japanese (Races 2 and 3) isolates of
Fusarium oxysporum f. sp. lactucae expressed as disease index (DI 0–100) at the end of the trials (from Gilardi et al. 2014). Reaction disease index 0–100; resistant (R) = 0–10;
partially resistant (PR) = 11–30; average susceptible (S) = 31–60; highly susceptible (HS) = 61–100. Reference cultivar Costa Rica, resistant to race 1 and susceptible to race 2 and
3; ‘Banchu Red Fire’ is resistant to race 2 and susceptible to races 1 and 3 (Fujinaga et al. 2003), while ‘Cavolo di Napoli’ is susceptible to all the three races as ‘Patriot.’

Plant Disease / September 2019 2163

hypothesis that the recent spread of this pathogen to some new hosts
is linked to climate change (Gullino et al. 2017a).
Verrucarin A biosynthesis has been found to increase significantly
at 35°C, while roridin E has increased for a carbon dioxide concentra-
tion of 800 ppm, thus showing a positive correlation between climate
change and macrocyclic trichothecene production (Siciliano et al.
2017b). Leaf spot, caused by A. verrucaria on spinach, was more se-
vere at higher temperatures and carbon dioxide concentrations.
In the case of leaf spot caused by P. roridum on cultivated rocket
(Eruca sativa), disease severity increased under eight different
temperature and carbon dioxide concentration combinations
(from 14–18°C to 26–30°C and with 400–450 or 800–850 ppm
of carbon dioxide), with high temperatures at both carbon dioxide
levels. Verrucarin A and roridin E mycotoxins were produced
under all the tested temperatures under high carbon dioxide conditions.
The maximum level of verrucarin A was found at 14–18°C, and the

Fig. 16. Reaction of several rocket cultivars used in the ready-to-eat sector artificially inoculated with two isolates of Fusarium oxysporum f. sp. raphani expressed as disease index
(DI 0–100) at the end of the trials. Data are the average of three trials (from Gilardi et al. 2014). Reaction disease index 0–100; resistant (R) = 0–10; partially resistant (PR) = 11–30;
average susceptible (S) = 31–60; highly susceptible (HS) = 61–100.

Table 5. Effect of nursery treatments on Fusarium wilt of lettuce on the cvs. Volare, Novelski, and Gentilina grown in an artificially infested peat substrate.
The data are expressed as disease severity 0–100 at the end of the greenhouse trials (from Gilardi et al. 2019).
cv. Novelski cv. Volare cv. Gentilina
Treatment Formulation Dosage a.i. Trial 1 Trial 2 Trial 3 Trial 4 Trial 3 Trial 4
Inoculated untreated control - - 64.4 fx 81.3 e 54.4 c 56.3 d 77.5 b 72.5 f
Noninoculated control - - 0.0 a 0.0 a 0.0 a 0.0 a 0.0 a 0.0 a
Bacillus subtilis QST713 Serenade Max 0.63 g/liter 29.4 de 41.9 cd 23.8 b 38.1 b-d 23.1 b 30.0 b-e
Trichoderma asperellum + Remedier 0.04 g/liter 31.3 de 41.3 cd 25.0 bc 40.0 cd 45.6 b 41.9 c-e
T. gamsii
Pseudomonas 9FC Agroinnova’ Pseudomonas 1 × 107 CFU/ml 33.1 e 52.5 de 21.9 b 36.9 b-d 36.3 b 48.1 ef
Fusarium oxysporum MSA 35 Agroinnova’ Fusarium 1 × 107 CFU/ml 28.8 c-e 46.9 cd 20.6 b 39.4 b-d 41.3 b 41.9 de
oxysporum
Acibenzolar-S-methyl Bion 50 WG 0.025 g/liter 26.3 c-e 30.0 b-d 17.5 b 31.9 bc 29.4 b 25.6 b-e
Potassium phosphite P:K 52:42 Alexin 1.3 + 1.06 g/liter 16.9 bc 35.6 cd 16.3 ab 33.1 bc 31.3 b 30.6 b-e
Phosethyl-Al Aliette 1.6 g/liter 12.5 b 26.3 bc 12.5 ab 28.1 bc 37.5 b 29.4 b-e
Green composty Ant’s compost 2015 V 10% 19.4 b-d 14.4 b 13.8 ab 19.4 b 29.4 b 20.0 b-d
Green compostz Ant’s compost 2015 V 1 kg/m2 25.0 c-e 26.9 bc 16.3 ab 23.1 bc 41.3 b 19.4 bc
Green compost y Compost 214 10% 28.1 c-e 33.1 cd 15.0 ab 24.4 bc 33.3 b 32.5 b-e
Animal bone biochary ABC 1% 25.0 c-e 36.3 cd 19.4 b 27.5 bc 46.7 b 41.9 de
Azoxystrobin Ortiva 0.19 g/liter 4.4 a 30.0 bcd 5.6 a 25.6 bc 31.3 b 15.0 b
x
Values in the same column followed by the same letter are not significantly different, according to Tukey’s HSD test (P = 0.05).
y
Applied at sowing at 1 or 10% by mixing in the plug-tray in nursery.
z
Applied by mixing in the soil before transplanting at 1 kg/m2.

2164 Plant Disease / Vol. 103 No. 9

maximum roridin E production was detected at 26–30°C, with
800–850 ppm of carbon dioxide for both toxins (Bosio et al. 2017).
Moreover, climate change is expected to affect strategies for dis-
ease control. For instance, it can reduce host resistance because some
resistance genes are temperature sensitive and may indirectly affect
the efficacy of applied agrochemicals under warmer temperatures
(Coakley et al. 1999; Garrett et al. 2006; West et al. 2012).
A positive trend for fresh cut products is also expected in the
future, with consumers expected to continue to show a positive
attitude toward such products and a willingness to pay. Recent stud-
ies carried out in the European Union highlighted the similarities in
preferences of consumers across countries and the relevance of
shelf life and food safety attributes in orienting choices (Baselice
et al. 2017). Consumers look for good taste and a convenient pur-
chase. They have also become more aware of social and environ-
mental issues. More integrated social and certification programs
will permit an increased sharing of information along the total supply
chain.

Table 6. Summary of the effect of increased temperature and CO2 on different pathosystems, evaluated under controlled environment facilities (modified
from Gullino et al. 2018)
Host (environmental
conditions tested)
Basil (400–450and 800–850
ppm CO2; 18–30°C)
Wild rocket (400–450 and
800–850 ppm CO2;
14–30°C)
Spinach (400–450 and
800–850 ppm CO2;
14–30°C)
Cultivated rocket (400–450
and 800–850 ppm CO2; 14
to 30°C)
Cultivated rocket (400–450
and 800–850 ppm CO2;
14–26°C)
Leaf beet (400–450 and
800–850 ppm CO2;
18–30°C)
Lettuce (400–450 and
800–850 ppm CO2;
14–26°C)
Basil (400–450 and 800–850
ppm CO2; 18–26°C)
Wild rocket (400–450 and
800–850 ppm CO2;
18–26°C)
Lettuce (400–450 and
800–850 ppm CO2; 18 to
26°C)
Cultivated rocket (400–450
and 800–850 ppm CO2;
18–30°C)
Pathogen (disease and type)
Peronospora belbahrii
(downy mildew, biotroph)
Fusarium equiseti (leaf spot,
necrotroph)
Albifimbria verrucaria (leaf
spot, necrotroph)
Paramyrothecium roridum
(leaf spot, necrotroph)
Alternaria sp. Leaf spot,
necrotroph)
Phoma betae (leaf spot,
necrotroph)
Allophoma tropica (leaf spot,
necrotroph)
Colletotrichum
gloeospoiroides (black spot,
necrotroph)
Alternaria sp. (leaf spot,
necrotroph)
Fusarium oxysporum f. sp.
lactucae (Fusarium wilt,
necrotroph)
Fusarium oxysporum
conglutinans (Fusarium wilt,
necrotroph)
Influence on diseases of
Temperature CO2 Overall effect on disease
Decrease at 26–30°C Increase for high levels Positive interaction between T
and CO2
Increase for high T Increase for high levels Increase, with positive
interaction between T and
CO2
Increase for high T No effect Increase, with positive
interaction between T and
CO2
Increase for high T No effect Increase, with positive
interaction between T and
CO2
Increase for high T No effect No interaction
Decrease at 26–30°C Increase for high levels Increase, with positive
interaction between T and
CO2
Increase at 22–26°C, Increase at 22–26°C Increase, with positive
decrease at 26–30°C interaction between T and
CO2 at 22–26°C
Increase for high T Increase for high levels Increase, positive interaction
between high T and CO2
Increase for high T Increase for high levels Increase
Increase for high T No effect Increase, positive interaction
between high T and CO2
Increase for high T Increase for high levels Increase, positive interaction
between high T and CO2

Table 7. Effects of increased temperature and CO2 evaluated under controlled environment facilities on mycotoxin production (modified from Gullino
et al. 2018)
Host (environmental Mycotoxin(s) Effect of increased T and/or CO2 and their
conditions tested) Pathogen produced interaction Reference
Spinach (400–450 and Albifimbria Verrucarin A Increase with temperature. No effect of CO2. Siciliano et al. 2017b
800–850 ppm CO2; verrucaria
14–30°C) Roridin E Increase at 14–18°C under 800–850 ppm CO2
Cultivated rocket Paramyrothecium Verrucarin A Increase at 14–18°C under 800–850 ppm CO2 Bosio et al. 2017
(400–450 and roridum
800–850 ppm CO2; Roridin E Increase at 26–30°C under 800–850 ppm CO2
14–30°C)
Cultivated rocket Alternaria sp. (leaf Tenuazonic acid Increase at 22–26°C under 800–850 ppm CO2 Siciliano et al. 2017a
(400–450 and spot, necrotroph)
800–850 ppm CO2;
14–26°C)
Alternariol and No effect
alternariol
monomethylether
Tentoxin Increase at 14–18°C, 400–450 ppm, and
18–22°C, 800–850 ppm CO2

Plant Disease / September 2019 2165

 To be successful in the marketplace, new technologies must be
better and cheaper than existing ones. Quality is what differentiates
companies in the marketplace, and this is considered highly propri-
etary and confidential information by the industry. This makes re-
search funding in this area difficult for university and government
personnel, as many processors prefer to develop proprietary process-
es in-house to assure confidentiality (Gorny 2005). More space for
public research in this sector exists in the field of food safety, since
any foodborne illness outbreak affects an entire food category and
not a single company. Consequently, fresh-cut processors are more
willing to collaborate and fund safety research than quality research.
Among research priorities, there is a need for new varieties that are
not only appealing to consumers but also resistant to the most frequent
diseases, not only for lettuce and spinach but also in the case of minor
leafy vegetables, such as rocket and lamb’s lettuce. In addition, seed
companies should invest more in the adoption of all measures needed
to prevent the spread of diseases throughout infected seeds.
For disease management, in most cases, an IPM approach is
needed and the success of this production sector strongly relies on
the presence of a well-trained extension service.
Acknowledgments
The authors would like to thank all the coworkers (Sara Franco-Ortega, Slavica
Matić, Giuseppe Ortu, Ilenia Siciliano, Ilenia Pintore, Walter Chitarra, Ilario Fer-
rocino, Federico Berta, Incoronata Luongo, Stefano Demarchi, Guido Martano,
and Gabriele Zerbini) who provided excellent support through the years and
Andrea Masino for drawing the figures of this manuscript. Thanks to Marco Omo-
dei, Raffaele Rocchetti, Marco Ferrari, Fausto Caserio, and Diego Scarpa for help-
ing us to keep good connections with the farmers. Finally, thanks to the reviewers
for improving the manuscript.
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 Maria Lodovica Gullino
Maria Lodovica Gullino is a professor of plant pathology and director of the Center of Competence
Agroinnova at the University of Torino. She has been president of the Italian Association for Crop Pro-
tection (AIPP, 1999–2004), the Italian Association of the Agrarian Societies (AISSA, 2002–2004), the
International Society for Plant Pathology (ISPP, 2008–2013), and the Italian Society for Plant Pathol-
ogy (2017–present). Her research interests cover plant disease management, plant and food biose-
curity, effects of climate change on plant diseases, and food safety and security. She is co-author of 23
books and over 800 scientific papers. She is Fellow of the American Phytopathological Society (APS)
and of the ISPP. She has been and is responsible for many research projects funded by the European
Union (FP 5, FP6, FP7, Horizon 2020, Tempus, Life, Europaid), NATO, several ministries, regional
governments, and enterprises. Some of the projects are related to agriculture in developing countries
and emerging economies. She has organized national and international meetings and workshops in
the field of plant disease management, as well as courses, at national and international level, for train-
ing technicians and researchers working in the extension service in the field of IPM. She founded Agri-
NewTech S.r.l., an academic spin-off and was CEO until 2011. She is also a professional journalist
and writer of popular books aimed at attracting people at large and children to science.

Giovanna Gilardi
Giovanna Gilardi is a senior technician at the Centre of Competence Agroinnova at the University of
Torino. She received an M.S. degree in agricultural sciences in 1998 and a Ph.D. in plant pathology in
2017 at the same university. Since the beginning, her research has focused on sustainable disease
management of vegetable crops, with special interest in soil disinfestation. Since 2002, she has
worked on biology, epidemiology, and management of diseases of leafy vegetables for the ready-
to-eat sector. In this field, she developed a solid expertise, becoming an important reference for
growers and extension services.

Angelo Garibaldi
Angelo Garibaldi is an emeritus professor at the University of Torino and president of the Centre of
Competence Agroinnova. He is involved in research in the field of plant disease management, dis-
eases of ornamental crops, and biology and epidemiology of emerging diseases on horticultural crops.
He has been president of the Associazione Fitopatologica Italiana (AFI, 1986–1990), dean of the Fac-
ulty of Agriculture (1990–1996) and vice-chancellor of the University of Torino (1996–2004). He did
manage many international and national research projects, funded by the European Union, different
ministries and agencies, and has always been strongly involved in technology transfer. He is an author
and/or co-author of eight books and over 1,000 scientific articles. He founded AgriNewTech S.r.l., an
academic spin-off.

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