Overview of Potyvirus resistance in watermelon 1

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1 Overview of Potyvirus resistance in watermelon 1 N. Guner 1 and T.C. Wehner 2* 1 Sakata Seed America Inc., SR 82, Ft. Myers, FL Department of Horticultural Science, North Carolina State University, Raleigh, NC * Corresponding author todd_wehner@ncsu.edu Keywords: ZYMV (Zucchini yellow mosaic virus), WMV (Watermelon mosaic virus), PRSV-W (Papaya ringspot virus watermelon strain), Citrullus lanatus Abstract Watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] is a major cucurbit crop that accounted for 7.5 % of the world area devoted to vegetable production in Potyviruses are a major limiting factor in commercial watermelon production worldwide. The major viruses affecting watermelon are Papaya ringspot viruswatermelon strain (PRSV-W), Watermelon mosaic virus (WMV), and Zucchini yellow mosaic virus (ZYMV). Sources of resistance to PRSV-W have been reported. These were PI (plant introduction) accessions from South Africa (PI , PI , PI ), from Zimbabwe (PI , PI , PI ), from Botswana (PI ), and from Nigeria (PI ). A single recessive gene controls resistance to PRSV-W, with the gene symbol prv. Resistance to WMV is a quantitative trait in watermelon, with approximately 3 major loci involved. PI is resistant to ZYMV, and is also moderately resistant to WMV. The USDA germplasm collection of 1613 PI accessions was screened for resistance to the Florida strain of Zucchini yellow mosaic virus (ZYMV-FL). A high level of resistance to ZYMV-FL was found in several accessions: PI , PI , PI , PI , PI , PI , PI , PI , and PI The study also confirmed the resistance of PI , PI , PI , and PI that was reported previously. Resistance of PI was confirmed to the three potyviruses PRSV-W, WMV, and ZYMV, so it will be useful in the development of multiple-virus resistant cultivars. Inheritance of resistance to Zucchini yellow mosaic virus-china strain (ZYMV-CH) and ZYMV-FL in PI was reported to be controlled by a single recessive gene. Further research is needed to determine whether resistance genes for ZYMV-FL in PI and in PI are allelic. INTRODUCTION Watermelon (Citrullus lanatus (Thunb.) Matsum. & Nakai) is a major cucurbit crop that accounts for 7.5 % of the world area devoted to vegetable production in Worldwide, watermelons are grown on over 3.7 million ha and produce more than 83 million Mg of fruit. A rough estimate of annual world value of watermelon exceeds $15 billion. Watermelon is grown in more than 96 countries worldwide. China is the world leader in watermelon production with 70.3 % of the total 1 Cucurbitaceae 2008, Proceedings of the IX th EUCARPIA meeting on genetics and breeding of Cucurbitaceae (Pitrat M, ed), INRA, Avignon (France), May th,

2 production in Other leading countries are Turkey (4.7 %), Iran (2.3 %), the United States (2.2 %), and Egypt (1.7 %) (FAO 2003). Watermelon has the highest lycopene content among fresh fruits and vegetables; watermelon contains 60 % more lycopene than tomato. Lycopene in the human diet is associated with prevention of heart attacks and certain cancers. Watermelon rind contains an important natural compound called citrulline, an amino acid that the human body makes from food. Citrulline is found in high concentration in the liver, and is involved with athletic ability and functioning of the immune system (Perkins-Veazie et al. 2001). Plant diseases caused by viruses are a major limiting factor in commercial watermelon production worldwide. Around the world, over 10 viruses are known to be a problem in watermelon production (Provvidenti 1986). The major viruses affecting watermelon are Papaya ringspot virus-watermelon strain (PRSV-W, formerly Watermelon mosaic virus-1), Watermelon mosaic virus (WMV, formerly Watermelon mosaic virus-2), and Zucchini yellow mosaic virus (ZYMV). All three viruses are non-persistently transmitted by many species of aphids, and mixed infections are common (Adlerz and Crall 1967; Mohr 1986; Provvidenti 1991; Wehner et al. 2001). Virus diseases are destructive to the watermelon crop, and are difficult to control. Plants infected with viruses lose their photosynthetic capacity and subsequently display stunted growth, deformed fruit, and early mortality (Sherf and Macnab 1986). Chemical control of the insect vectors is not usually sufficient for control of the disease. Cultural controls such as mineral oil sprays, light-reflective surfaces, and cross protection with weak PRSV-W isolates show limited effectiveness and require additional input costs. Genetic resistance is a simple, effective and efficient means of controlling virus diseases (Provvidenti 1993). In this review, we will describe briefly the major potyviruses affecting watermelon production worldwide with new resistant sources and the genes. PRSV-W Resistance PRSV-W affects all agricultural species of the Cucurbitaceae and is of great economic importance because of its destructiveness (Provvidenti 1993). PRSV-W was first described by Webb and Scott (1965) from Sri Lanka (Bateson et al. 2002). For many years, PRSV-W was considered to be the distinct potyvirus, WMV-1 (Webb and Scott 1965). However, the PRSV-P (papaya) and PRSV-W (watermelon) isolates were found to be indistinguishable serologically (Gonsalves and Ishii 1980) and now are considered to be strains of Papaya ringspot virus (Purcifull et al. 1984; Purcifull and Hiebert 1979; Baker et al. 1991). The main reason for the early confusion about the taxonomic status of the W isolate was that it does not infect papaya. However, the P isolates infect cucurbits as well as papaya (Provvidenti 1993). PRSV-W is transmitted in a non-persistent manner by 24 aphid species in 15 genera with Myzus persicae, Aulacorthum solani, Aphis craccivora, and Macrosiphum euphorbiae as natural vectors. PRSV-W is a potyvirus (family Potyviridae) whose genome consists of unipartite, single-stranded, linear RNA. Its total genome size is 12 kb, and the genome codes for 8 proteins. PRSV-W induces pinwheel and scroll types of cytoplasmic cylindrical inclusions in infected host cells (Purcifull et al. 1984). Type W isolates are reported to infect 38 species in 11 genera 446

3 of Cucurbitaceae, and two species of Chenopodiaceae, with watermelon, cucumber (Cucumis sativus L.), melon (Cucumis melo L.), and squash (Cucurbita spp.) among the commercially important natural hosts. The virus is not seed transmitted. It appears to overwinter in wild species of Cucurbitaceae and Chenopodiaceae (Purcifull and Hiebert 1979). Symptoms of severe PRSV-W infection in cucurbits include leaves with mosaic, puckering, blistering, and size reduction, vines that are stunted, and fruit that are small, knobby, malformed, and mottled. PRSV-W causes significant yield reduction in watermelon, cucumber, melon, and squash and other cultivated cucurbits (Provvidenti 1993). Researchers have screened cucurbit species other than watermelon for resistance to PRSV-W, and the inheritance of the resistance has been determined. Sources of resistance to PRSV-W have been reported in cucumber, melon, and squash. PRSV-W resistance is controlled by a single dominant gene in cucumber (Wai and Grumet 1995) and a single dominant gene in melon (Pitrat and Lecoq 1983). In squash, resistance to PRSV-W is controlled by a single recessive gene in C. moschata (Bolanos-Herrera 1994) and by three partially-dominant genes in C. maxima (Maluf et al. 1997). Sources of resistance to PRSV-W have been also reported in watermelon. The most extensive screening of the USDA watermelon germplasm collection (total of 1650 accessions) for resistance to PRSV-W was done by Strange et al. (2002). In this screening, the most virulent PRSV-W isolate, 2052 was used (Guner et al. 2002). PRSV-W resistance was reported in three PI accessions from South Africa (PI , PI , PI ), in three PI accessions from Zimbabwe (PI , PI , PI ), one accession from Botswana (PI ) and one accession from Nigeria (PI ). All of the resistant accessions except PI are C. lanatus var. citroides, whereas PI is C. lanatus var. lanatus. The inheritance of resistance to PRSV-W was studied in three C. lanatus var. citroides accessions: PI , PI , and PI (Guner et al. 2008a). Three susceptible parent lines, 'Allsweet', 'Calhoun Gray', and 'New Hampshire Midget', were crossed with resistant accessions to develop F 1, F 2, and BC 1 generations for six families. A single recessive gene was found to control resistance to PRSV-W in all three resistant PI accessions. A test of allelism indicated that resistance to PRSV-W in the three PI accessions was due to the same gene. The gene symbol prv was proposed for PRSV-W resistance in PI , PI , and PI in watermelon. WMV Resistance Watermelon mosaic virus (formerly Watermelon mosaic virus 2, family Potyviridae) is one of the most destructive viruses affecting watermelon production in the United States and worldwide. The virus was first described by Webb and Scott (1965). WMV naturally infects members of Cucurbitaceae, Chenopodiaceae, Malvaceae and Leguminosae families (Shukla 1994). Resistance to WMV in C. lanatus and in C. colocynthis has been reported. Resistance to WMV in watermelon has been reported to vary with virus strain. In India, 59 watermelon cultivars were found to be resistant to WMV (Bhargava and Bhargava 1976). However, Sowell and Demski (1969) reported later that all 59 cultivars tested were susceptible in their test. 447

4 Three PI accessions (PI , PI , and PI ) were reported free of symptoms in a field test in Florida (Adlerz and Crall 1967). 'Egun' (C. lanatus) (Webb 1977) and some Egusi accessions (PI and PI ) were also reported resistant to WMV. Gillaspie and Wright (1993) evaluated a total of 670 Citrullus accessions for resistance to WMV. Selections from 10 C. lanatus accessions (PI , PI , and PI from Zaire; PI , PI , and PI from South Africa; PI from India; PI , PI , and 'Egun' from Nigeria were reported resistant in both field and greenhouse tests. Five C. colocynthis PI accessions (PI , PI , PI , and PI from Iran, and PI from Morocco) had some resistance in both field and greenhouse tests (Gillaspie and Wright 1993). C. colocynthis can be intercrossed with C. lanatus, and is a useful source of resistance. However, a major problem with C. colocynthis is that it is not useful commercially, and the flesh is bitter (Munger et al. 1984), so a lot of work is required to transfer traits to adapted cultivars. Xu et al (2004) reported that PI , which is resistant to ZYMV, was moderately resistant to WMV. Strange et al. (2002) also reported that PI was resistant to Papaya ringspot virus watermelon strain. The high tolerance to WMV was controlled by at least three recessive genes. Broad-sense heritability was high (0.84 to 0.85, depending on the cross), and narrow-sense heritability was low to high (0.14 to 0.58, depending on the cross). ZYMV Resistance ZYMV is one of the most destructive viruses in watermelon production (Nameth et al. 1985). ZYMV infects all the agriculturally important species of the Cucurbitaceae (Provvidenti 1991). ZYMV was first described in 1981 in squash grown in northern Italy (Lisa and Dellavalle 1981). ZYMV spread within a decade to the major cucurbit-producing regions worldwide. ZYMV is a potyvirus, with flexuous rods about 750 nm long containing a single strand of RNA. ZYMV is spread in a non-persistent manner by many aphid species, and is easily transmitted mechanically. In areas where cucurbits are not grown continuously, the virus overwinters on wild species. Natural infection appears to be limited to members of the Cucurbitaceae, but members of 11 families of dicotyledons are considered diagnostic hosts. At least 25 strains of ZYMV have been identified. They differ in virulence, symptom severity, and the ability to induce symptoms on plants carrying resistance genes (Desbiez and Lecoq 1997). The major strains in the United States are the Connecticut (ZYMV-CT) and the Florida strain (ZYMV-FL) (Brown 2001). In their research, Xu et al. (2004) used the China strain of ZYMV. Symptoms of severe ZYMV infection in Cucurbits include yellow mosaic, stunting, blistering and laminar reduction on leaves. Fruit become mottled and malformed, remain small, and develop knobby areas (Provvidenti 1996). ZYMV causes yield reduction in watermelon, squash, melon, cucumber and other cultivated cucurbits (Nameth et al. 1985). The severity of infection depends on the age of plants at infection, the strain of ZYMV involved, and the environment, particularly temperature (Desbiez and Lecoq 1997). Researchers have screened other cucurbit species for resistance to ZYMV, and the inheritance of the resistance has been determined. Sources of resistance to ZYMV 448

5 have been reported in cucumber, melon, and squash. ZYMV resistance is controlled by a single recessive gene in cucumber (Kabelka et al. 1997), a single dominant gene in melon (Pitrat and Lecoq 1984), and a single dominant gene in squash (Munger and Provvidenti 1987; Paris et al. 1988; Gilbert-Albertini et al. 1993; Brown 2001). The watermelon germplasm collection has been screened for resistance to ZYMV, and resistant PI accessions have been identified (Boyhan et al. 1992; Provvidenti 1991; Guner et al. 2008b). Provvidenti (1991) reported ZYMV resistance in four PI accessions of watermelon from Zimbabwe (PI , PI , PI , and PI ). The ZYMV resistance in the four resistant PI accessions in watermelon appeared to be specific to the Florida strain (ZYMV-FL). Some accessions of the Egusi watermelon type originating in Nigeria (PI and PI ) were reported resistant to ZYMV, and the resistance was not specific to virus strain. However, the resistance was temperature dependent, and was expressed best in warm or hot climates (Provvidenti 1986). The USDA germplasm collection of 1613 PI accessions, as well as 41 watermelon cultivars were screened for resistance to the Florida strain of Zucchini yellow mosaic virus (ZYMV-FL) A high level of resistance to ZYMV was found in several PI accessions. These new resistant PI accessions were PI , PI , PI , PI , PI , PI , PI , PI , and PI The study also confirmed the resistance of PI , PI , PI and Egun (PI ). However, the resistance of PI , PI , PI , and PI as reported by Provvidenti (1991) was not confirmed. Those PI accessions had only moderate resistance to the Florida strain (ZYMV-FL) used in the study (Guner et al. 2008b). Provvidenti (1991) reported that resistance in PI was conferred by a single recessive gene, which he named zym. Boyhan et al. (1992) reported additional sources of resistance to ZYMV in PI , PI , and Egun (PI ). They also confirmed ZYMV resistance in PI and PI Xu et al. (2004) studied inheritance of Zucchini yellow mosaic virus-china strain (ZYMV-CH) in PI They reported that resistance to ZYMV-CH was conferred by a single recessive gene, for which the symbol zym-ch was suggested. A high level of resistance to ZYMV-FL in Egun (PI ) was probably controlled by a single recessive gene. ZYMV isolates have been reported to differ in pathogenicity, aphid transmissibility, and serological or molecular properties (Lecoq and Purcifull 1992; Desbiez and Lecoq 1997). Thus, it is important to determine whether the two ZYMV strains are the same, and whether the two resistance genes are the same. Further research is needed to determine whether the two genes controlling resistance to ZYMV-FL are allelic. CONCLUSIONS In the United States, the USDA watermelon germplasm collection has been extensively screened for resistance to PRSV-W, ZYMV and WMV. All virus resistance data on PI accessions was reported to The Germplasm Resources Information Network (GRIN) for future use by researchers. GRIN is on the world wide web at Several resistant PI accessions are being used by watermelon breeders to develop resistant cultivars. Other countries have 449

6 watermelon germplasm collections that could be screened for improved sources of resistance. For example, the Vavilov Institute in Russia has more than 2,500 accession collected from around the world. Literature cited Adlerz WC, Crall JM (1967) Epidemiology of control of watermelon mosaic virus. Florida Agr Exp Sta Ann Rep 403 Baker CA, Lecoq H, Purcifull DE (1991) Serological and biological variability among Papaya ringspot virus type-w isolates in Florida. Phytopathology 81: Bateson MF, Lines RE, Reville P, Chaleeprom W, Ha CV, Gibbs AJ, Dale JL (2002) On the evolution and molecular epidemiology of the potyvirus Papaya ringspot virus. J General Biology 83: Bhargava B, Bhargava KS (1976) Reaction of some cucurbits to seven strains of watermelon mosaic virus. Indian Phytopathol 29: Bolanos-Herrera AB (1994) Inheritance of virus resistance in Cucurbita moschata and C. maxima. MS thesis. Dept. of Vegetable Crops, Cornell Univ., Ithaca, NY. Boyhan G, Norton JD, Jacobsen BJ, Abrahams BR (1992) Evaluation of watermelon and related germ plasm for resistance to zucchini yellow mosaic virus. Plant Dis 76: Brown RN (2001) Traditional and molecular approaches to zucchini yellow mosaic virus resistance in Cucurbita. PhD Thesis. Dept. of Horticulture, Oregon State University, Corvallis, Oregon. Desbiez C, Lecoq H (1997) Zucchini yellow mosaic virus. Plant Path 46: FAO (2003) Agricultural statistics for Food and Agriculture Organization of the United Nations, Gillaspie AG, Wright JM (1993) Evaluation of Citrullus sp. germ plasm for resistance to watermelon mosaic virus 2. Plant Dis 77: Gilbert-Albertini F, Lecoq H, Pitrat M, Nicolet JL (1993) Resistance of Cucurbita moschata to watermelon mosaic virus 2 and its genetic relation to resistance to zucchini yellow mosaic virus. Euphytica 69: Gonsalves D, Ishii M (1980) Purification and serology of Papaya ringspot virus. Phytopathology 70: Guner N, Wehner TC (2008) Inheritance of resistance to Zucchini yellow mosaic virus in watermelon. J Hered (in review). Guner N, PesicVan-Esbroeck Z, Wehner TC (2008a). Inheritance of resistance to Papaya ringspot virus-watermelon strain in watermelon. J Hered (in review). Guner N, PesicVan-Esbroeck Z, Wehner TC (2008b) Screening for resistance to Zucchini yellow mosaic virus in 1654 watermelon cultivars and plant introduction accessions. Crop Sci. (in review). Guner N, Strange EB, Wehner TC, PesicVan-Esbroeck Z (2002) Methods for screening watermelon for resistance to Papaya ringspot virus type-w. Scientia Hort 94: Kabelka E, Ullah Z, Grumet R (1997) Multiple alleles for zucchini yellow mosaic virus resistance at zym locus in cucumber. Theor Appl Genet 95: Lecoq H, Purcifull DE (1992) Biological variability of potyviruses, an example: zucchini yellow mosaic virus. Arch Virol Suppl 5: Lisa V,. Dellavalle G (1981) Characterization of two potyviruses from zucchini squash. Phytopathology 100: Maluf WR, Pereira JJ, Figueira AR (1997) Inheritance of resistance to the Papaya ringspot virus watermelon strain from two different PI accessions of winter squash Cucurbita maxima Duch. Euphytica 94: Mohr HC (1986) Watermelon breeding. Breeding vegetable crops. p AVI Publishing Co. 450

7 Munger HM, More TA, Awni S (1984) A preliminary report on screening watermelon for resistance to watermelon mosaic viruses 1 and 2. Cucurbit Genet Coop Rep 7: Munger HM, Provvidenti R (1987) Inheritance of resistance to zucchini yellow mosaic virus in Cucurbita moschata. Cucurbit Genet Coop Rpt 10: Nameth ST, Dodds JA, Paulus AO, Kishaba AK (1985) Zucchini yellow mosaic virus associated with severe diseases of melon and watermelon in Southern California desert valleys. Plant Dis 69: Paris HS, Cohen S, Burger Y, Yoseph R (1988) Single-gene resistance to zucchini yellow mosaic virus in Cucurbita moschata. Euphytica 37: Perkins-Veazie P, Collins JK, Pair SD, Roberts W (2001) Lycopene content differs among red-fleshed watermelon cultivars. J Science Food Agric 81: Pitrat M, Lecoq H (1983) Two alleles for watermelon mosaic virus 1 resistance in melon. Cucurbit Genet Coop Rep 6: Pitrat M, Lecoq H (1984) Inheritance of zucchini yellow mosaic virus resistance in Cucumis melo L. Euphytica 33: Provvidenti R (1993) Resistance to viral diseases of vegetables. In Kyle MM (ed). Timber Press, Inc. Portland, OR. Provvidenti R (1991) Inheritance of resistance to the Florida strain of zucchini yellow mosaic virus in watermelon. HortScience 26: Provvidenti R (1986) Reactions of PI accessions of Citrullus colocynthis to zucchini yellow mosaic virus and other viruses. Cucurbit Genet Coop Rep 9: Provvidenti R (1996) Zucchini yellow mosaic virus. In Compendium of Cucurbit diseases (Zitter TA, Hopkins DL, Thomas CE, eds), APS Press, St. Paul (MN, USA2) P. 44 Purcifull DE, Edwardson JR, Hiebert E, Gonsalves D (1984) Papaya ringspot virus. CMI/AAB Descriptions of plant viruses. No 292 Purcifull DE, Hiebert E (1979) Serological distinction of watermelon mosaic virus isolates. Phytopathology 69: Sherf AI, Macnab AA (1986) Vegetable diseases and their control (Second edition). John Wiley and Sons. Shukla DD, Ward CW, Brunt AA (1994) The potyviridae. Cab International. Wallingford, Oxon UK. Sowell G, Demski JW (1969) Susceptibility of watermelon cultivars to watermelon mosaic virus-2. Plant Dis Rep 53: Strange EB, Guner N, Pesic-VanEsbroeck Z, Wehner TC (2002) Screening the watermelon germplasm collection for resistance to Papaya ringspot virus type-w. Crop Sci 42: Wai T, Grumet R (1995) Inheritance of resistance to the watermelon strain of Papaya ringspot virus in the cucumber line TMG-1. HortScience 30: Webb RE, Scott HS (1965) Isolation and identification of watermelon mosaic viruses 1 and 2. Phytopathology 55: Webb SE, Tyson RV (1997) Evaluation of virus resistant squash varieties. Proc Fla State Hort Soc 110: Wehner TC, Shetty NV, Elmstrom GW (2001) Breeding and seed production. In Watermelons. Characteristics, production, and marketing (Maynard DN, ed), ASHS Press, Alexandria (VA, USA) p Xu Y, Kang D, Shi Z, Shen H, Wehner TC (2004) Inheritance of resistance to zucchini yellow mosaic virus and watermelon mosaic virus in watermelon. J Hered 96:

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