Journal of Plant Pathology (2014), 96 (2), 227-242 Edizioni ETS Pisa, 2014 Romay et al. 227

Offered Review

CUCURBIT CROPS AND THEIR VIRAL DISEASES IN LATIN AMERICA AND THE CARIBBEAN ISLANDS: A REVIEW

G. Romay1,2, H. Lecoq1 and C. Desbiez1

1INRA, UR407 Unité de Pathologie Végétale, 84140 Montfavet, France 2Fundación Instituto de Estudios Avanzados (IDEA). Carretera Nacional Hoyo de la Puerta, Sartenejas, Caracas 1080, Venezuela

SUMMARY 83,429,409 tons of melon, watermelon, cucumber and squash, while the USA is the main producer in the West- Cucurbit crops are cultivated throughout the world. ern Hemisphere with 4,602,370 tons (FAOSTAT, 2012). Melon (Cucumis melo L.), cucumber (Cucumis sativus L.), Cucurbit crops are often threatened by diseases of fun- watermelon (Citrullus lanatus (Thumb.) Mat. et Nak.), gal, bacterial and viral origin (Sitterly, 1972) and pests, squash and pumpkin (Cucurbita spp.) are the major crops. such as the pumpkin caterpillars (Diaphania spp.) and the In Latin America and the Caribbean islands (LAC) cucur- melon fly (Bactrocera cucurbitae Coquillet), are also seri- bits are consumed as a part of the daily diet since pre-Co- ous constraints to their cultivation (Peter and David, 1991; lumbian times, when some species such as Cucurbita pepo Duyck et al., 2004; Dhillon et al., 2005; HansPetersen et L., Cucurbita moschata Duch. and Cucurbita maxima Duch. al., 2010). Aphids, whiteflies and thrips can become serious were domesticated by American Indians. In LAC, cucurbit limitations to cucurbit production through the extensive crops have become export commodities and a source of damage they provoke, but also through the transmission of income for several countries, in addition to their role in viral disease (Brown et al., 1995; Morse and Hoddle, 2006; local consumption. The increase of area devoted to cu- Powell et al., 2006). curbit crops and the intensification of production has led At least 59 viruses infecting cucurbits are known to the emergence of severe viral epidemics that threaten (Lecoq and Desbiez, 2012), whose outbreaks have led the sustainability of these cultures. This paper reviews the to significant yield and quality losses to these crops on a cucurbit viruses described in the region and their impact. worldwide basis (Flock and Mayhew, 1981; Desbiez and In addition, the potential of different measures to control Lecoq, 1997; Brown et al., 2001; Lecoq and Desbiez, 2012). the most frequent cucurbit viruses in LAC is discussed. This review examines the current situation of cucurbit production in Latin America and the Caribbean islands Key words: Cucurbitaceae, plant viruses, cucurbit pro- (LAC), with special emphasis on viral diseases that affect duction, Latin American countries these crops, and the perspectives for their control.

INTRODUCTION ORIGIN OF MAJOR CUCURBIT PLANTS CULTIVATED IN LATIN AMERICA AND THE CARIBBEAN ISLANDS Cucurbits represent one of the most important vegeta- bles for human consumption throughout the world. Cu- Cucumber (Cucumis sativus). Cucumber is widely curbit species are members of the family Cucurbitaceae grown in cool temperate regions because it is better adapt- that roughly includes 120 genera and 800 species, which ed to low temperatures than other cucurbits (Paris et al., are predominantly tropical plants though some, such as 2012). Cultivated cucumbers are usually monoecious. India Bryonia spp. and Alsomitra spp., are adapted to temperate is the centre of origin of cucumber that has been culti- climates (Teppner, 2004). Four major cucurbit crops are vated there for at least 3,000 years and introduced later in economically important worldwide: melon (Cucumis melo China and Europe (Leppik, 1966) and, in the 15th century, L.), cucumber (Cucumis sativus L.), watermelon (Citrul- in the Western Hemisphere by Columbus (Robinson and lus lanatus (Thumb.) Mat. & Nak.), squash and pumpkin Decker-Walters, 1997). The most closely related species to (Cucurbita spp.) (Robinson and Decker-Walters, 1997). C. sativus is the southeast Asian Cucumis hystrix Chackr. Global production of cucurbits cultivated in the world (Renner et al., 2007; Sebastian et al., 2010). C. sativus is is 151,212,210 tons. China is the main producer with the seventh plant species whose genome (243.5 Mb) has been sequenced. This is expected to provide a remark- Corresponding author: G. Romay Fax : + 58.212.9035003 able increase of new findings for its genetic improvement E-mail: [email protected] (Anonymous, 2009) 228 Cucurbit viruses in Latin America Journal of Plant Pathology (2014), 96 (2), 227-242

Melon (Cucumis melo). Melon is the other important comprises eight species (Bisognin, 2002), among which crop in the genus Cucumis. Its genome has recently been C. lanatus subsp. lanatus (Tsamma and citron type) and sequenced, which will contribute to further investigations C. lanatus subsp. vulgaris (sweet-dessert watermelon group) involving evolution and genetic improvement (García-Mas (Levi et al., 2012). Although a large number of commer- et al., 2012). The C. melo genome has a size of 454 Mb, cial varieties of watermelon are being released each year, while its mitochondrial genome (2,740 Kb) is the largest their genetic diversity is low, increasing the risks of pest among plant mitochondrial genomes, i.e. up to 100 times and disease threats. Hence, the great interest to enhance the size of a typical animal mitochondrial genome (Rodrí- genetic diversity using new germplasm coming from dif- guez-Moreno et al., 2011). The difference in genome size ferent geographical regions (Zhang et al., 2012). between C. melo and C. sativus is probably due in part to transposon amplification in the melon genome (García- Squash (Cucurbita maxima, C. moschata, C. pepo). Mas et al., 2012). Africa is considered as the centre of ori- The genus Cucurbita comprises 12-14 different species gin of melon because of the large number of African wild of American origin and a distribution ranging from the species (Robinson and Decker-Walters, 1997), whereas USA to Argentina (Sanjur et al., 2002). Along with corn Central Asia and China are regarded as secondary cen- (Zea mays L.) and beans (Phaseolus spp), squashes were tres (Leppik, 1966). This assumption was supported by domesticated in the Americas, playing a crucial role for the chromosome numbers: melon and 30 other African the development of American Indian agriculture (Carter, species in the genus Cucumis have a chromosome number 1946). As stated by Paris (2000), six species were origi- of X = 12, whereas C. sativus has a chromosome number nally listed by Linnaeus in the genus Cucurbita on the of X = 7 (Luan et al., 2008). However, recent phylogenet- basis of phenotypic features. Afterwards, four of them ic analyses have shown that C. melo may have an Asian (C. pepo, C. verrucosa, C. melopepo, C. ovifera) were re- rather than an African origin, suggesting the Himalayan assigned to the species C. pepo and the other two were region as the ancestral area for progenitor populations of re-located in the genus Lagenaria and Citrullus. The great melon and cucumber. Moreover, a sister species of melon polymorphism exhibited by C. pepo may have led Linnae- is the Australian Cucumis picrocarpus F. Muell. whose di- us to identify four different species instead of a unique, vergence from melon occurred roughly 2.8 million years but polymorphic, species. Years later, the botanist A.N. ago (Sebastian et al., 2010). Duchesne demonstrated, on the basis of inability to hy- bridize and produce fertile offspring, that several forms Watermelon (Citrullus lanatus). Watermelon is more of Cucurbita belonged to the polymorphic C. pepo and produced than any other cucurbit in the world with that, more interestingly, two other Cucurbita forms were 73,313,777 tons according to latest reports. In Europe, wa- unable to hybridize with C. pepo, therefore, they were termelon production is slightly exceeded that of another considered as distinct species that were named C. maxima cucurbit, cucumber (FAOSTAT, 2012). Watermelon origi- and C. moschata (Paris, 2000). C. pepo is the northern- nates from Africa (Robinson and Decker-Walters, 1997). most species of the three aforementioned Cucurbita, the The presumed ancestor of the modern cultivar C. lanatus northwest of Mexico and the south-east of the USA being includes wild annual forms referred to as C. lanatus subsp. thought to be domestication centres of this species (Cart- lanatus var. caffer (Schrad.) Mansf., which are natives to er, 1946; Nee, 1990; Sanjur et al., 2002). Archeological the Kalahari Desert (Southern Africa). However, the find- studies in Mexico provided evidence of C. pepo and other ing of 5000-year-old seeds of wild watermelon in an ar- wild cucurbits cultivation as early as 8,750 BC, almost chaeological site in southwest Libya raises new discussions 60% of them being wild Cucurbita species and C. pepo about the origin, distribution and domestication history the only cultivated species (Whitaker and Cutler, 1971). of this species (Wasylikowa and van der Veen, 2004). In Three subspecies are recognized: C. pepo subsp. fraterna Asia, watermelon was introduced to India and China in (only found in wild form), C. pepo subsp. pepo (only found about the 9th and 12th century, respectively, in Europe by in cultivation) and C. pepo subsp. texana (found in culti- the Moors during their conquest of Spain (Dane and Liu, vation and wild form). The last two are more genetically 2007) and in the Americas by the Spaniards and rapidly related to each other (Gong et al., 2012). C. moschata is spread throughout the continent (Robinson and Decker- thought to originate from the middle American area, Walters, 1997). According to Romão (2000), a secondary from which it spread southward and northward (Carter, centre of watermelon diversity is northeast Brazil where 1946). The wild ancestor of C. moschata is unknown, slave trading might have reached 18 millions people com- though molecular DNA analyses suggest that it may be ing from Africa in two major groups, Bantu and Sudanese. localized in lowland northern South America (Sanjur et The same author indicates that African watermelon eth- al., 2002). Archeological studies carried out in northern novarieties could be grown in the same areas, may be in Peru revealed the presence of C. maxima and C. moschata slaves gardens, leading to new segregants and recombinant between 1,800 BC and 1,100 AD, but interestingly, these forms during the long period of slave trading. C. lanatus species were found to be chronologically different, C. is the only cultivated species of the genus Citrullus which maxima being the older one (West and Whitaker, 1979). Journal of Plant Pathology (2014), 96 (2), 227-242 Romay et al. 229

Table 1. Production of major cucurbit crops in Latin America and the Caribbean islands.

Region Melon Squash Cucumber Watermelon Tons Surface Tons Surface Tons Surface Tons Surface (ha) (ha) (ha) (ha) North Americaa 561,681 21,418 522,388 32,100 477,366 15,653 1,036,800 44,040 Central America 874,781 39,635 12,310 5,600 82,567 3,042 39,145 15,405 Caribbean 85,606 9,374 446,915 68,967 127,318 12,231 65,480 7,829 South America 929,926 55,502 776,317 47,535 134,251 8,784 2,839,364 162,516 Total 2,451,994 125,929 1,757,930 154,202 824,502 39,710 3,980,789 229,790 Source: FAOSTAT, 2012; aData relative to Mexican cucurbit production.

As suggested by this finding, C. maxima might have been Rica, Mexico, Brazil and Puerto Rico for local consump- replaced by C. moschata probably due to ecological and tion and export (Abdelnour and Rocha, 2008). Chayote cultural factors. C. maxima is thought to be a native of the was cultivated by pre-Columbian Aztec civilizations and humid lowland of Bolivia and warmer temperate regions its centre of origin seems to be between Mexico and Gua- of South America, where Cucurbita andreana Naudin, the temala, where wild species of Sechium have been found wild progenitor of C. maxima, was originally described (Newstrom, 1991). The genus Sechium was initially con- (Sanjur et al., 2002). C. maxima was not present in North sidered as monotypic containing only S. edule, but eight America until the 18th century when it was introduced to species have now been described in this genus (Robinson north-eastern USA by sailing ships from South America and Decker-Walters, 1997). (Robinson and Decker-Walters, 1997). Two other species are also cultivated in America, Cucurbita ficifolia Bouché and Cucurbita argyrosperma Huber. C. ficifolia is com- PRODUCTION OF MAJOR CUCURBITS IN LATIN mon in the mountains from northern Mexico to northern AMERICA AND THE CARIBBEAN ISLANDS Argentina and Chile (Nee, 1990). C. ficifolia can be used as rootstock to confer chilling tolerance and improved Estimates show that global production of cucur- plant growth to cucumbers grown under low light inten- bits in LAC is 9,012,215 tons harvested from 549,631 ha sity (Zhou et al., 2007). C. argyrosperma is little known (FAOSTAT, 2012), watermelon being the major species. outside Central and North America, where some cultivars As shown in Table 1, Mexico, the only Latin country in are grown for their large nutritious seeds rather than for North America, is the greatest producer of cucumber the flesh (Nee, 1990). among LAC countries. Interestingly, melon production Another cucurbit often found in archaeological explo- in Central America is similar to that in South America, rations carried out in the Western Hemisphere is bottle in spite of the remarkable difference in the total surface gourd (Lagenaria siceraria (Molina) Standl.) (Whitaker and given over to this crop in either region. This fact shows Cutler, 1971; West and Whitaker, 1979; Whitaker, 1981; the outstanding role of some cucurbits in the economy of Erickson et al., 2005; Duncan et al., 2008). This cucurbit several countries in the region, where cucurbit export is was thought to be domesticated in the Western Hemi- one of the significant source of income. The USA is the sphere due to the older archaeological evidence gathered main importer of cucurbits to supply consumer demands from this part of the world (Nee, 1990). Afterwards, an during winter. Thus, Mexico exports around 30% of its African origin was proposed for L. siceraria, based on melon production to the USA (Hernández-Martínez et al., the diversity of wild species in the genus Lagenaria and 2006; García-Salazar et al., 2011), while Guatemala devotes the morphological and genetic characterization of a wild its melon production almost totally to the USA market (de population of L. siceraria (Robinson and Decker-Walters, Cara et al., 2008). In Guatemala, the melon area harvested 1997; Decker-Walters et al., 2004). Wild species were sup- in 2000 was 5,880 ha. Ten years later, it was 22,777 ha, posed to have moved from Africa to the Americas 9,000 rising by 387.4% (FAOSTAT, 2012). In Brazil, melon ex- years ago through their fruits floating across the ocean ports have been favoured by the increasing development (Decker-Walters et al., 2004). However, subsequent archae- of multinational supermarket chains creating scaling-up ological studies suggested that L. siceraria was brought to of opportunities for growers with capacity to support ini- the Americas 10,000 years ago by Paleoindian populations tial investments, whereas small farmers lack substantial from Asia rather than by oceanic crossing of floating fruits improvements in organization and technology to confront from Africa (Erickson et al., 2005). these challenges (Farina, 2000). By contrast, Argentina was the third greatest producer of squash in the world during Chayote (Sechium edule (Jacq.) Sw.). Although cha- the early 1980s, with approximately 31,000 ha harvested yote is not one of the major cucurbit crops in the world, (Robinson and Decker-Walters, 1997) while in 2010, the this plant is grown in several LAC countries such as Costa harvested area was 19,600 ha so that this country dropped 230 Cucurbit viruses in Latin America Journal of Plant Pathology (2014), 96 (2), 227-242

Table 2. Cucurbit-infecting viruses in Latin America and Caribbean islands

Virus Vector Countries Reference Cucumber mosaic virus Aphids Argentina, Brazil, Chile, Costa Lastra, 1968; Quiot et al., 1971; Thomas, 1981; Delgadillo- Rica, Guadeloupe; Honduras, Sánchez et al., 1989, Rivera et al., 1991; Espinoza and McLeod, Martinique, Mexico, 1994; Yuki et al., 2000; Prieto et al., 2001; Paz-Carrasco and Monserrat, Panama, Puerto Wessel-Beaver, 2002; Arneodo et al., 2005; Herrera et al., 2006 Rico, Venezuela Papaya ringspot virus W Aphids Brazil, Costa Rica, Honduras, Lastra, 1968; Quiot et al., 1971; Delgadillo-Sánchez et al., 1989; Guadeloupe, Martinique, Rivera et al., 1991; Espinoza and McLeod, 1994; Yuki et al., 2000; Mexico, Panama, Venezuela Herrera et al., 2006 Zucchini yellow mosaic virus Aphids Argentina, Brazil, Chile, Costa Nameth et al., 1985; Hernández et al., 1989; Espinoza and Rica, Dominican Republic, McLeod, 1994; Desbiez and Lecoq, 1997; García et al., 2000; Honduras, Guadeloupe, Yuki et al., 2000; Prieto et al., 2001; Herrera et al., 2006 Martinique, Mexico, Panama, Puerto Rico, Venezuela Watermelon mosaic virus Aphids Argentina, Brazil, Chile, Costa Lastra, 1968; Delgadillo-Sánchez et al., 1989; Rivera et al., 1993; Rica, Honduras, Mexico, Hernández et al., 2000, Yuki et al., 2000; Prieto et al., 2001; Paz- Puerto Rico, Venezuela Carrasco and Wessel-Beaver, 2002; Herrera et al., 2006 Zucchini tigré mosaic virus Aphids Costa Rica, Guadeloupe, Quiot-Douine et al., 1986; Romay et al., 2014a Martinique, Venezuela Squash mosaic virus Beetles Brazil, Chile, Honduras, Lastra, 1968; Delgadillo-Sánchez et al., 1989; Thomas, 1981; Mexico, Monserrat, Puerto Espinoza and McLeod, 1994; Prieto et al., 2001; Moura et al., Rico, Venezuela 2001; Paz-Carrasco and Wessel-Beaver, 2002 Squash leaf curl virus Whiteflies Mexico Flock and Mayhew, 1981; McCreight and Kishaba, 1991 Cucurbit leaf crumple virus Whiteflies Mexico Brown et al., 2000 Melon chlorotic leaf curl virus Whiteflies Costa Rica, Guatemala, Brown et al., 2001; Karkashian et al., 2002; Ala-Poikela et al., Mexico, Nicaragua 2005; Hernández-Zepeda et al., 2007 Melon chlorotic mosaic virus Whiteflies Venezuela Ramírez et al., 2004 Tomato yellow leaf curl virus Whiteflies Cuba Martínez-Zubiaur et al., 2003 Cucurbit yellow stunting Whiteflies Mexico Brown et al., 2007 disorder virus Beet pseudo-yellows virus Whiteflies Costa Rica Hammond et al., 2005 Melon yellowing-associated Whiteflies Brazil Nagata et al., 2005 virus Tobacco ringspot virus Nematodes Mexico Delgadillo-Sanchez et al., 1989 Zucchini lethal chlorosis virus Thrips Brazil Pozzer et al., 1996; Nagata et al., 1998 Melon severe mosaic virus Thrips Mexico Ciuffo et al., 2009 Tomato spotted wilt virus Thrips Brazil, Chile, Puerto Rico Silveira et al., 1985; Prieto et al., 2001; Paz-Carrasco and Wessel- Beaver, 2002 Melon necrotic spot virus Fungi Guatemala, Honduras, de Cara et al., 2008; Herrera-Vásquez et al., 2010 Panama, Mexico Squash necrosis virus Fungi Brazil, Martinique Lin et al., 1983, Lecoq, 2003 Chayote mosaic virus Beetles Costa Rica Hord et al., 1997 out of the top 10 squash producers in the world. However, survival and spreading from one susceptible host to an- during the same period the Argentinan harvested area of other (Hull, 2002). The knowledge of the way in which soybean increased from approximately 2,000,000 ha to a particular virus is disseminated throughout the field is 18,130,800 ha increasing by ca. 890% becoming one of indispensable to develop adapted control strategies. There- the most important sources of income (FAOSTAT, 2012). fore, a list of the major cucurbit viruses detected in LAC is presented according to their respective vector types.

CUCURBIT VIRUSES REPORTED IN LATIN AMERICA Aphid-borne viruses. 1. Cucumber mosaic virus (CMV) AND THE CARIBBEAN ISLANDS is the type member of the genus Cucumovirus (family Bromoviridae). CMV genome size is approximately 8 kb At least 21 cucurbit-infecting viruses have been report- consisting of three linear positive-sense single stranded ed from LAC (Table 2), whose symptoms are very variable, RNA molecules (Bujarski et al., 2012) which are packaged i.e. mosaic, deformation, chlorosis, curling and yellowing in separate icosahedral virions. The virus is transmitted of the leaves, vein clearing and vein banding, stunting of by aphids in a non-persistent manner (Nault, 1997), is di- the plants and deformation of fruits (Fig. 1). Plant viruses vided in two subgroups (I and II) based on nucleotide se- are obligate parasites that usually depend on a vector for quence identity and serological properties and is reported Journal of Plant Pathology (2014), 96 (2), 227-242 Romay et al. 231

Fig. 1. Symptoms associated with viral diseases of cucurbit crops A. Leaf curling and stunting caused by Melon chlorotic mosaic virus (MeCMV) in melon. B. Rugose mosaic caused by Melon chlorotic mosaic virus (MeCMV) in melon. C. Mosaic and leaf de- formation caused by Papaya ringspot virus (PRSV-W) in melon. D. Vein clearing and slight mosaic caused by Papaya ringspot virus (PRSV-W) in watermelon. E. Mosaic caused by Zucchini yellow mosaic virus (ZYMV) in squash. F. Severe leaf deformation and mosaic caused by Zucchini yellow mosaic virus (ZYMV) in zucchini squash. G. Mosaic caused by Cucumber mosaic virus (CMV) in melon. H. Vein banding caused by Squash mosaic virus (SqMV) in melon. 232 Cucurbit viruses in Latin America Journal of Plant Pathology (2014), 96 (2), 227-242 to infect over 1000 species in more than 85 botanical Field surveys of cucurbit viruses have shown PRSV-W families (Hull, 2002). Since CMV has an extensive host as prevalent in Costa Rica (Rivera et al., 1993). In Brazil, range, there are numerous records of susceptible species extensive viral surveys in cucurbit fields from Northern to from several plant families in LAC. This review will focus South-eastern regions in different years have shown that on reports about CMV-infected cucurbits only (Table 2). PRSV-W is widespread with a remarkable predominance CMV induces leaf mosaic, fruit yield reduction and stunt- (>40%) compared with other cucurbit viruses (Yuki et al., ing in melon and cucumber, while zucchini squash shows 2000; Oliveira et al., 2000; Moura et al., 2001; Halfeld-Vie- severe mosaic, leaf distortion and yellows spots (Lecoq ira et al., 2004; Silveira et al., 2009). In contrast, PRSV-W and Desbiez, 2012). Although CMV is often found infect- has not been reported, so far, in the southernmost coun- ing cucurbits at a low frequency in LAC (Lastra, 1968; tries, Argentina and Chile, where other cucurbit potyvi- Yuki et al., 2000; Moura et al., 2001; Paz-Carrasco and ruses are present (García, 2000; Prieto et al., 2001). Wessel-Beaver, 2002; Félix-Gastélum et al., 2007; Romay et al., 2014b), some reports from Venezuela and Costa Ri- 3. Zucchini tigré mosaic virus (ZTMV). ZTMV was ca show that CMV is able to causes severe losses in melon firstly described in Guadeloupe as the T strain of PRSV when in mixed infection with a potyvirus (Acosta et al., (PRSV-T) due to the particular symptoms of “tiger” stripe 1973; Rivera et al., 1991). Synergistic interactions between pattern on zucchini plants and its biological relationships CMV and the potyvirus ZYMV (see below) have led to with PRSV, though PRSV-T was antigenically distinct severe outbreaks in cucurbit fields (Lecoq et al., 1981). from PRSV-W (Quiot-Douine et al., 1986). However, re- In potyviruses, HC-Pro protein causes the suppression cent sequence comparisons indicate that PRSV-T is actu- of post-transcriptional gene silencing to prevent plant ally a new potyvirus species closely related to but distinct defence responses (Kasschau and Carrington, 1998) and, from PRSV, occurring in Guadeloupe, Martinique, Costa among other functions, is also involved in genome am- Rica and Venezuela. ZTMV has probably long been over- plification and viral long-distance movement (Kasschau looked because of its close relationship to PRSV, the lack et al., 1997). Thus, it was suggested that, when in mixed of discriminating diagnostic tools and its high frequency infection with a potyvirus, CMV could take advantage of of co-infections with PRSV (Romay et al., 2014a). the HC-Pro functions to increase its systemic infection in the plant (Gal-On, 2007). 4. Zucchini yellow mosaic virus (ZYMV), a potyvi- rus first observed in Italy in the early 1970s, 10 years 2. Papaya ringspot virus (PRSV) belongs to the genus later was widely distributed in cucurbit crops around Potyvirus (family Potyviridae), whose members have flexu- the world with devastating consequences (Desbiez and ous filamentous particles containing a ca.10 kb positive- Lecoq, 1997). Usually, disease symptoms are severe sense single stranded RNA genome with a VPg protein mosaic, deformation of leaves or fruits and stunting of at the 5’ end and a poly(A) sequence at the 3’ end (Hull, plants. However, one of the main features of ZYMV is 2002). Potyviruses are transmitted by aphids in a non- the great biological variability among its strains whereby persistent manner. They can be experimentally transmit- differences in host range as well as symptoms severity or ted by mechanical inoculation and some are seed-trans- nature (necrosis or wilting reactions) can be expected mitted (Adams et al., 2012a). PRSV is a worldwide virus (Lecoq and Desbiez, 2012). Based on molecular analyses, that infects mainly cucurbits and papaya with devastat- three distinct groups of ZYMV are recognized (groups ing consequences. Although serologically and genetically A, B and C), all isolates from the Western Hemisphere indistinguishable, two PRSV types have been described known so far belonging to group A (Coutts et al., 2011a). based on biological behaviour: PRSV type P (PRSV-P) in- In LAC, ZYMV was first detected in Mexico (Nameth et fecting papaya and to a lesser extent cucurbits and PRSV al., 1985) but current records show that it occurs in nu- type W (PRSV-W), formerly referred as WMV-1, infect- merous LAC countries, the same as the earlier reported ing cucurbits but not papaya (Purcifull et al., 1984). It is PRSV-W and CMV (Table 2). Prevalence of ZYMV in worth mentioning that PRSV-P is the major constraint for LAC field crops seems to be variable, while virus surveys papaya but it is very uncommon in cucurbit crops, con- from Mexico showed that it occurred with a frequency trary to PRSV-W (Bateson et al., 2002). However, PRSV-P higher (ca. 30%) than PRSV-W, Watermelon mosaic virus was found naturally infecting a cucurbit weed (Momordica (WMV) and CMV in two distinct years (Félix-Gastélum charantia L.) in Southern Jamaica (Chin et al., 2007). In et al., 2007). In Puerto Rico and Venezuela, ZYMV in- experimental conditions a single mutation at the amino cidence was comparable to that of PRSV-W, with a fre- acid position 27 of the NIaPro protein of PRSV is able to quent presence of mixed infections (Paz-Carrasco and elicit a host-switching of PRSV from cucurbits to papaya Wessel-Beaver, 2002; Romay et al., 2014b). Interestingly, or vice versa (Chen et al., 2008). Cultivated cucurbits in- both potyviruses had similar frequency but PRSV was fected by PRSV-W display symptoms of severe mosaic, more prevalent in cucurbit weeds than ZYMV, prob- blistering, malformations of leaves and discoloration as ably due to its longer time of adaptation to local endem- well as deformations of fruits (Lecoq and Desbiez, 2012). ic plants. In Brazil, PRSV is still the most important Journal of Plant Pathology (2014), 96 (2), 227-242 Romay et al. 233 cucurbit virus though an increasing frequency of ZYMV endemic to squash throughout the southwestern USA and has been observed (Silveira et al., 2009). Mexico (McCreight and Kishaba, 1991). This New World begomovirus has now spread to several countries in the 5. Watermelon mosaic virus (WMV) is another potyvi- Middle East (Desbiez and Lecoq, 2012). rus reported from several LAC countries (Table 2). This virus is an important constraint to cucurbit production 2. Cucurbit leaf crumple virus (CuLCrV) is another be- in temperate and Mediterranean climatic conditions, and gomovirus first found in California (USA) in volunteer can also be responsible for severe diseases in non-cucurbits watermelons in commercial melon fields. The symptoms crops such as beans, pea and vanilla (Lecoq and Desbiez, displayed by infected plants were yellowing, leaf curl and 2008). However, as a whole, WMV is rare or absent in crumpling (Guzman et al., 2000). During the same period, tropical regions (Lecoq and Desbiez, 2012). Three main whitefly-infested pumpkins and melons from Arizona and groups of WMV have been identified based on molecu- Texas (USA), and Coahuila (Mexico) showed begomovi- lar analysis, the American isolates falling into the second rus-like symptoms which were associated with a new be- group referred to as G2 (Lecoq and Desbiez, 2012). Symp- gomovirus species named Cucurbit leaf curl virus (Brown toms associated with WMV infections can be mosaic, vein et al., 2000). This virus was recently synonymized with banding, filiformism and reduction in the size of the leaves CuLCrV by the International Committee on Taxonomy and may vary according to the host and the viral isolate. of Viruses (ICTV) (Adams and Carstens, 2012). CuLCrV WMV is a common virus in cucurbit crops in Chile, where is common in melons grown in the fall planting period in it was reported to cause significant yield losses (Prieto et southwestern United States (McCreight et al., 2008). To al., 2001). Its incidence in cucurbit crops from Costa Rica, date, no new reports have come from Mexico or from any Puerto Rico, Mexico and Venezuela was estimated around other LAC country. 20% (Lastra, 1968; Rivera et al., 1993; Paz-Carrasco and Wessel-Beaver, 2002; Félix-Gastélum et al., 2007) although 3. Melon chlorotic leaf curl virus (MCLCuV) is a be- recent surveys in the latter country have disclosed a much gomovirus identified in 2000 in the Zacapa Valley of lower (ca. 3%) prevalence (Romay et al., 2014b). By con- Guatemala where it infects, with a 70 to 80% incidence, trast, the average incidence of this virus in Brazil, which melons that exhibit patchy foliar chlorosis, leaf curling, was estimated at about 10% (Yuki et al., 2000; Moura et and reduced fruit set (Brown et al., 2001). Zacapa Valley al., 2001; Halfeld-Vieira et al., 2004) had grown to approxi- is a large area dedicated almost exclusively to melon pro- mately 30% according to a more recent report (Silveira et duction for the international market (Brown et al., 2011), al., 2009). which makes MCLCuV a serious threat to the economy of the country. The very severe symptoms elicited by this Whitefly-borne viruses. 1. Squash leaf curl virus (SLCV) virus in melon and watermelon, contrast with the milder belongs to the genus Begomovirus, family Geminiviridae. syndromes caused by SCLV and CuLCrV, both of which The genome of most begomoviruses consists of two circu- infect the same cucurbit species (Idris et al., 2008). MCL- lar single-stranded DNA molecules, each ca 2.7 kb in size, CuV was recorded under the name of Squash yellow mot- referred to as DNA A and DNA B. However, some bego- tle virus from Costa Rica (Karkashian et al., 2002), where moviruses such as Tomato yellow leaf curl virus (TYLCV), it is widely distributed (Hernández et al., 2012) and is also have a single genomic component similar to DNA A of bi- present in Nicaragua (Ala-Poikela et al., 2005), and in the partite begomoviruses (Stanley et al., 2005). Most begomo- Yucatan peninsula of Mexico infecting watermelon and viruses are phloem-restricted and are transmitted by the squash (Hernández-Zepeda et al., 2007). whitefly Bemisia tabaci Genn. in a persistent manner (Na- vas-Castillo et al., 2011). Actually, B. tabaci is considered 4. Melon chlorotic mosaic virus (MeCMV) is the most as a complex of at least 24 indistinguishable species (Dins- southern cucurbit begomovirus so far reported from LAC. dale et al., 2010). The Middle East-Asia Minor 1 (MEAM1) It was found for the first time in Venezuela in melons show- whitefly, commonly referred as biotype B, is regarded as ing mosaic and chlorosis of the leaves (Ramírez et al., 2004) the most invasive species and efficient begomovirus vec- and, some years later, in watermelon in association with tor (De Barro et al., 2011). In the mid 1980s MEAM1 was a DNA alphasatellite molecule (MeCMA) (Romay et al., introduced in the Western Hemisphere where, within a 2010). Alphasatellites are self-replicating circular DNA few years, it displaced indigenous whiteflies in the USA molecules ca. 1.3 kb in size whose encapsidation, vector and several LAC countries (Perring et al., 1993; Morales, transmission and movement in the plant rely on their help- 2006). SLCV was first recorded in the USA and Mexico er virus. They had only been associated with Old World in the late 1970s, infecting zucchini squash (C. pepo) in monopartite begomoviruses (Nawaz-ul-Rehman and Fau- which it induces thickening of the veins, upward curling quet, 2009). However, new begomovirus-alphasatellite of the leaves, enations and stunting (Flock and Mayhew, associations, besides that of MeCMV-MeCMA, have re- 1981). Phylogenetic analyses indicate that SLCV belongs to cently been reported in the Americas (Paprotka et al., 2010). the “New World” begomovirus clade and is considered as To date, MeCMV is the major constraint to melon and 234 Cucurbit viruses in Latin America Journal of Plant Pathology (2014), 96 (2), 227-242 watermelon growing in Venezuela, where its infections have limited to the province of Cartago and the adjacent areas, an incidence of approximately 80% (Romay et al. 2014b). where the genetic variability of BPYV isolates appears low (Ramírez et al., 2008). 5. Squash leaf curl virus-like (SLCV-like). Several iso- lates of begomoviruses infecting cucurbits in El Salvador, 9. Melon yellowing-associated virus (MYaV) is a mem- Honduras and Colombia have partially been sequenced ber of the genus Carlavirus, family Betaflexiviridae. Car- showing a close relationship to SLCV (Brown et al., lavirus virions are slightly flexuous filaments of 600-700 2002; Morales, 2006). Further sequencings are needed to nm in length. Carlavirus genome consists of a linear, clarify the taxonomic position of these viruses that seem positive single stranded RNA (Adams et al., 2012b). Al- to be members of the same phylogenetic group, i.e. the though most carlaviruses are transmitted by aphids, two SCLV clade which includes also CuLCrV, MCLCuV and of them, Cowpea mild mottle virus (CPMMV) and MYaV MeCMV. are transmitted by B. tabaci in a semi-persistent manner (Navas-Castillo et al., 2011). MYaV has only been reported 6. Tomato yellow leaf curl virus (TYLCV) is a typi- form northeast Brazil, where it causes severe symptoms of cal monopartite begomovirus from the Old World that yellowing and mottling of older leaves in melon plantings infects mainly tomato. This virus was introduced in the (Nagata et al., 2005). Americas in the late 1980s, rapidly becoming the greatest threat to tomato production in the Caribbean (Morales 10. Squash vein yellowing virus (SqVYV) belongs to the and Anderson, 2001). Although TYLCV was isolated in genus Ipomovirus, family Potyviridae. The genome orga- Cuba from C. pepo exhibiting yellowing and curling of nization of ipomoviruses is similar to that of potyviruses, the leaves (Martínez-Zubiaur et al., 2003) and was also except that at the 5’ end of most ipomovirus genomes, in- found in other cucurbits in the Middle East (Anfoka et cluding SqVYV, there is a duplicated P1 and no HC-Pro al., 2009), there is no evidence of yield losses caused to (Li et al., 2008). Ipomoviruses are phylogenetically distinct cucurbit crops elsewhere. from potyviruses and their transmission is mediated by whiteflies instead of aphids (Adams et al., 2012a). SqVYV 7. Cucurbit yellow stunting disorder virus (CYSDV) is was first described in Florida (USA) infecting C. pepo a member of the genus Crinivirus, family Closteroviridae. where the main symptom observed was vein yellowing. Criniviruses have a genome of 15 to 18 kb consisting of It was also associated with vine decline and fruit rot in two linear positive-sense single stranded RNA molecules watermelon crops (Adkins et al., 2007). SqVYV has not yet encapsidated in very flexuous particles. They infect main- been detected in LAC. However, since the virus has been ly herbaceous plants inducing chlorosis and yellowing in identified in Indiana and South Carolina (USA) (Adkins et the leaves, as well as stunting. Criniviruses are transmit- al., 2011) the risk of its moving to the LAC region is high. ted by whiteflies in a semi-persistent manner (Martelli et SqVYV is efficiently transmitted by the MEAM1 whitefly al., 2012). CYSDV is transmitted by the whitefly B. tabaci (Adkins et al., 2007) which is widely distributed in LAC but not by the greenhouse whitefly (Trialeurodes vaporari- (Morales and Anderson, 2001; Morales, 2006). orum Westwood) nor by mechanical inoculation (Celix et al., 1996). In the Western Hemisphere, CYSDV was first Beetle-transmitted viruses. 1. Squash mosaic virus reported from southern Texas (USA) and northern Mexico (SqMV) is a member of the genus Comovirus, family Seco- (Kao et al., 2000). In 2006, this virus was associated to viridae. Its genome consists of two separately encapsid- severe outbreaks in cucurbits fields in USA and Mexico ated positive-sense single stranded RNA molecules with a reaching up to 100% incidence, while populations of B. 5’end-bound polypeptide (VPg) and a 3’ end poly(A) tail tabaci were variable ranging from 5 to 100 individuals per (Sanfaçon et al., 2012). In nature, comoviruses are trans- plant (Brown et al., 2007). In melon, watermelon and zuc- mitted by beetles when they regurgitate during feeding. chini squash, the symptoms associated with CYSDV infec- The beetles can retain viral particles for days or weeks tions are bright yellow and interveinal chlorosis of older and there is no evidence for a latent period following viral and mid-growth leaves (Brown et al., 2007). acquisition (Fulton et al., 1987). SqMV is also seed-borne in melon and squash with a mean transmission rate of ap- 8. Beet pseudoyellows virus (BPYV) is another species proximately 10% (Alvarez and Campbell, 1978). This virus of the genus Crinivirus which, unlike CYSDV, is transmit- can also be transmitted mechanically through pruning op- ted by the whitefly T. vaporariorum and can infect a large erations in the fields (Lecoq et al., 1988). Symptoms such number of plant species including weeds, ornamentals and as pronounced vein banding, mosaic and leaf deformation vegetables (Wisler et al., 1998). In LAC, BPYV has only can be induced by SqMV in melon and squash (Lecoq and been reported from Costa Rica associated with high infes- Desbiez, 2012). tations of whiteflies and severe yellowing and chlorosis of SqMV, along with WMV, is an important virus of cu- the leaves in squash and zucchini squash (Hammond et al., curbits in Chile (Prieto et al., 2001) as well as in some 2005). The presence of BPYV in Costa Rica seems to be USA areas (Jossey and Babadoos, 2008). The occurrence Journal of Plant Pathology (2014), 96 (2), 227-242 Romay et al. 235 of this virus is very low in Brazil, although it has been ex- 2. Zucchini lethal chlorosis virus (ZLCV) is a tospovirus ceptionally observed to reach 56% incidence in the field that was first isolated in Brazil from zucchini squash and (Alencar et al., 2012). In Puerto Rico, SqMV was detected cucumbers in São Paulo state and the Federal District, with a prevalence of 30%, whereas the infection rate in respectively (Pozzer et al., 1996; Nagata et al., 1998). In cu- Venezuela is very low (less than 6%) (Lastra, 1968; Her- cumber, ZLCV causes mottling, yellowing, and vein band- nandéz et al., 1989; Romay et al., 2014b). ing of the leaves (Nagata et al., 1998) and it was found as- sociated with important yield losses of marketable fruits in 2. Chayote mosaic virus (ChMV) belongs to the genus extensive areas of zucchini cropping (Bezerra et al., 1999). Tymovirus, family Tymoviridae. Tymoviruses have a linear, Currently, there is no evidence of ZLCV occurrence in positive-sense single stranded RNA genome of about 6.3 any country other than Brazil. ZLCV is transmitted by kb (Hull, 2002). Tymoviruses are transmitted mechani- Frankliniella zucchini (Nakahara and Monteiro, 1999) and cally and, in nature, in a semi-persistent manner and a its host range is mainly restricted to the family Cucurbita- low efficiency by beetles of the families Chrysomelidae ceae (Bezerra et al., 1999) unlike TSWV, which has a much and Curculionidae (Dreher et al., 2012). ChMV has only broader host range. been described in Costa Rica infecting chayote plants (Hord et al., 1997). The host range of the virus is limited 3. Melon severe mosaic virus (MeSMV) is a tospovirus to cucurbit species, which exhibit mosaic and leaf corruga- infecting melon, watermelon, cucumber and zucchini in tion, whereas symptomless infections are observed in other several states of Mexico. The virus can be mechanically hosts belonging to botanical families such as Solanaceae transmitted to cucurbit and solanaceous plants. Although and Amaranthaceae (Bernal et al., 2000). In Costa Rica, its natural vector is unknown, the western flower thrips chayote had been traditionally cultivated as a backyard (F. occidentalis) was observed in melon plants exhibiting crop, but in the 1980s it became an important crop for the mosaic, leaf blistering, leaf deformation, and fruit splitting export market (Flores, 1989), which has likely favoured the (Ciuffo et al., 2009). development of viral diseases. Fungus-transmitted viruses 1. Melon necrotic spot virus Nematode-transmitted viruses. Tobacco ringspot virus (MNSV) a member of the genus Carmovirus, family Tom- (TRSV) is the type species of the genus Nepovirus, family busviridae, has a genome consisting of a molecule of linear Secoviridae. Members of this genus have a genome organi- positive-sense single stranded RNA of approximately 4 Kb. zation similar to that of comoviruses, are widely distribut- Several carmovirus species are soil-borne and are readily ed in temperate regions and most of them are transmitted transmitted mechanically under experimental and natural persistently by nematodes (Sanfaçon et al., 2012). TRSV conditions. MNSV is transmitted by Olpidium bornovanus can be associated with a RNA satellite of small size, about (Sahtiyanci) Karling (Campbell et al., 1995; Rochon et al., 359 nucleotide long, which interferes with virus replica- 2012). The presence of MNSV and O. bornovanus was as- tion and disease symptoms (Hull, 2002). TRSV induces sociated with melon vine decline in Guatemala (de Cara et chlorotic spots, systemic ringspots, severe leaf deforma- al., 2008). In Panama, MNSV was reported to cause stem tion, mottling, and stunting in squash plants (Abdalla et necrosis, necrotic spots on the leaves and wilting of plants al., 2012). In the mid 1980s, TRSV was found in cucurbits in commercial melon crops (Herrera et al., 2006). The vi- in Mexico (Delgadillo-Sanchez et al., 1989), but its field rus was also detected in cucurbits in Mexico and Hondu- incidence was not assessed. ras (Herrera-Vazquez et al., 2010) but it was not found in Venezuela (Romay et al., 2014b). MNSV has also been re- Thrips-transmitted viruses. 1. Tomato spotted wilt virus ported to be seed-borne in melon through a vector-assisted (TSWV) is the type species of the genus Tospovirus, fam- seed transmission mechanism (Campbell et al., 1996). ily Bunyaviridae. Tospoviruses have spherical or pleomor- phic particles and a genome comprising three molecules of 2. Squash necrosis virus (SqNV) is a tentative carmovirus negative or ambisense single stranded RNA (Plyusnin et al., species found in Brazil (Lin et al., 1983) and in Martinique 2012). Tospoviruses are transmitted by thrips in a circula- Island (Lecoq, 2003). SqNV causes systemic necrotic spots tive and propagative manner (Hull, 2002). Virus acquisi- in squash and is transmitted by some strains of O. bornova- tion occurs during the first instar larval stages and viral nus (Campbell et al., 1995). particles are transmitted to plants during feeding of adults (Jones, 2005). TSWV has a host range of about 1100 species belonging to 85 botanical families (Parrella et al., 2003). PERSPECTIVES FOR THE MANAGEMENT AND Although TSWV is an important pathogen of tomato, CONTROL OF CUCURBIT VIRUSES IN LAC lettuce and sweet pepper rather than cucurbits (Jones, 2005) it was reported infecting these crops in Brazil, A management program for viral diseases begins Chile and Puerto Rico (Prieto et al., 2001; Paz-Carrasco with an accurate assessement of the viral threats secured and Wessel-Beaver, 2002). through extensive field surveys. Development of new 236 Cucurbit viruses in Latin America Journal of Plant Pathology (2014), 96 (2), 227-242 simple and reliable detection methods as well as the gener- WMV and PRSV than those in which cucurbit plots were alized use of diagnostic kits already available will allow the surrounded with grain sorghum (Damicone et al., 2007). carrying out of extensive new surveys in LAC. This will However, whereas this practice may be useful in small provide an updated and comprehensive picture of cucur- scale cultivation, its use in extensive areas (e.g. melon for bit-infecting viruses in the region. The success of disease export) is less practical. Plastic mulches were also shown management also relies on the understanding of the epide- to delay the onset of infections by thrips-, whitefly- and miological processes (Jeger, 2004). Virus epidemics involve aphid-borne viruses (Abou-Jawdah et al., 2000; Momol et interactions between the virus, host plants, vectors and the al., 2004; Adkins et al., 2011; Lecoq and Desbiez, 2012). environment (Jones et al., 2010). Thus, by managing some Silver plastic mulches are more efficient than black plas- of these factors a sustainable control is feasible. tic mulches to reduce vector populations (Simmons et al., The use of insecticides to reduce whitefly populations 2010; Coutts et al., 2011b), but the higher cost of silver has led to a significantly fewer presence of SqVYV symp- plastic mulch is a limiting factor to its wide use in some toms in watermelon crops in Florida (USA) (Adkins et cucurbit-growing areas (Adkins et al., 2011). al., 2011). However, insecticide treatments against aphid Control of alternative hosts of viruses or vector popu- vectors are generally not efficient for controlling cucurbit lations is another strategy for reducing virus disease inci- potyviruses (Webb and Linda, 1993; Coutts et al., 2011b; dence. In tropical and subtropical regions of LAC, the ef- Lecoq and Desbiez, 2012). Mineral oils, at weekly inter- ficiency of this control strategy is affected by the environ- vals, have been used to reduce the incidence of viruses mental conditions that favour the presence of weeds and non-persistently transmitted by aphids (Loebenstein and cultivated cucurbits for the whole year round. However, Raccah, 1980), as they seem to interfere with retention the removal of potential reservoirs including weeds, volun- of potyvirus particles on the aphid stylet, reducing viral teer cucurbit plants, crop remnants and plants with viral acquisition (Desbiez and Lecoq, 1997). Nevertheless, in symptoms is recommended (Coutts et al., 2011b). Suscep- experimental melon fields of California (USA), mineral oil tible crop-free periods have been a useful measure to re- sprays did not reduce virus spread to tolerable level when duce the impact of TYLCV in Dominican Republic where inoculum pressure was high (Umesh et al., 1995). processing tomato production was dramatically affected Cross-protection is another method for plant virus con- in the 1990’s (Salati et al., 2002). This type of measures trol, where pre-infection with a mild strain of a virus may can contribute to sustainable cucurbit production, but protect the hosts from severe challenging strains of the their implementation must take into account the impact same virus. The mild ZYMV-WK strain has been success- on countries like Guatemala, Costa Rica and Honduras, fully used to control severe strains of this virus in France, where cucurbit crops are important sources of income. Italy, Israel, Taiwan, Turkey, the United Kingdom and the The use of virus-resistant cultivars is one of the most USA (Desbiez and Lecoq, 1997). However, ZYMV-WK valued and simple strategies to control plant viruses. Du- was not efficient to prevent infections caused by very di- rable resistance to ZYMV has been introgressed in cu- vergent ZYMV isolates from Réunion Island (Lecoq and cumber (resistance conferred by the zym gene), while a Desbiez, 2012). In Israel, an efficient method was devel- resistance in melon (Zym gene) is easily overcome (Lecoq oped for inoculating the ZYMV-WK strain in cucurbit and Desbiez, 2012). The cucumber cv. Taichung Mou Gua plantlets on a large scale. (Yarden et al., 2000). (TMG) that possessed the zym gene was shown to be com- Cross-protection against severe strains of PRSV was pletely resistant to 34 Venezuelan ZYMV isolates, whereas also successfully achieved using mild strains (referred to one of these isolates completely overcame the resistance of as PRSV-W-1 and PRSV-W-2) under greenhouse and field melon line PI 414723, which also possessed the Zym gene, condition in Brazil (Rezende and Pacheco, 1998). How- suggesting a low durability of the melon resistance if used ever, subsequent cross-protection assays, using the mild in the field (Romay et al., 2014b). A high level of resistance strain PRSV-W-1, showed that a severe strain of PRSV to ZYMV is also available in squash (C. moschata). It was could still be detected in the non-inoculated upper leaves, introduced in zucchini squash (C. pepo) by interspecific suggesting competition for viral replication sites between crosses, but the resistance level is only partial in this host PRSV strains (Freitas and Rezende, 2008). Cross-protec- (Lecoq and Desbiez, 2012). For PRSV, resistance sources tion is an alternative to control plant viral diseases that have been identified in melon, cucumber, squash and wa- requires long-term and extensive studies to validate the use termelon (Lecoq et al., 1998; Maluf et al., 1997; Strange of a viral mild strain at an economical scale without risks et al., 2002), and commercial cucumber cultivars with re- of strain reversion towards a more severe form. sistance genes are already available (Lecoq and Desbiez, Cultural practices that tend to reduce viral epidemics 2012). In Brazil, several sources of resistance to PRSV in and damages can perform efficiently for many plant vi- squash and watermelon have been found and their inheri- ruses. Such practices attempt to prevent the interaction tance determined (Maluf et al., 1997; Oliveira et al., 2003; between the host plant, the vector and the viral source. Azevedo et al., 2012). Trials in which cucurbits and grain sorghum were inter- The crinivirus CYSDV is a relatively recent emerging cropped performed better in reducing field epidemics of plant virus (Navas-Castillo et al., 2011) so that efforts to Journal of Plant Pathology (2014), 96 (2), 227-242 Romay et al. 237 look for resistance sources are in progress. McCreight Taxonomy of Viruses, pp 1069-1089. Elsevier/Academic and Wintermantel (2011) identified a recessive gene in the Press, Amsterdam, The Netherlands. melon line PI 313970 (C. melo var. acidulus Naudin), which Adams M.J., Candresse T., Hammond J., Kreuze J.F., Martelli conferred a high level of resistance to CYSDV. A reces- G.P., Namba S., Pearson M.N., Ryu K.H., Saldarelli P., Yo- sive gene for resistance to CuLCrV was found in melon shikawa N., 2012b. Betaflexiviridae. In: King A.M.Q., Adams PI 2313970 (McCreight et al., 2008) and squash cultivars M.J., Carstens E.B., Lefkowitz E.J. (eds). Virus Taxonomy: partially resistant to SLCV are commercially available Ninth Report of the International Committee on Taxonomy of Viruses, pp 920-941. Elsevier/Academic Press, Amster- (Lecoq and Desbiez, 2012). To date, there are no reports dam, The Netherlands. of screenings for resistance sources to MCLCuV, in spite of Adkins S., Webb S.E., Achor D., Roberts P.D., Baker C.A., its presence in several countries from Latin America with 2007. Identification and characterization of a novel whitefly- intensive and extensive cucurbit production. transmitted member of the family Potyviridae isolated from Virus resistance mediated by genetically modified (GM) cucurbits in Florida. Phytopathology 97: 145-154. plants is now available for controlling some plant viruses. Adkins S., Webster C.G., Kousik C.S., Webb S.E., Roberts P.D., Squash cultivars expressing the coat protein gene of CMV, Stansly P.A., Turechek W.W., 2011. Ecology and manage- WMV and ZYMV and resistant to these viruses are cur- ment of whitefly-transmitted viruses of vegetable crops in rently grown in the USA (Lecoq and Desbiez, 2012). How- Florida. 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