FUSARIUM WILT IN SEEDLESS WATERMELONS. P. O. Box 159, Lane, Oklahoma LESREC, Salisbury, MD. SWFREC, Immokalee, FL

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1 FUSARIUM WILT IN SEEDLESS WATERMELONS B. D. Bruton 1, W. W. Fish 1, X. G. Zhou 2, K. L. Everts 2, P. D. Roberts 3 1 U S Department of Agriculture-Agricultural Research Service P. O. Box 159, Lane, Oklahoma bbruton-usda@lane-ag.org 2 University of Maryland LESREC, Salisbury, MD. 3 University of Florida, Department of Plant Pathology SWFREC, Immokalee, FL As a prelude to discussing Fusarium wilt in seedless watermelon, we wish to first briefly review the disease from a historical perspective. Fusarium wilt of watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai], caused by Fusarium oxysporum f. sp. niveum (E.F. Sm.) Snyd. & Hans., was first reported in the United States in 1894 (Smith, 1894). Historically, Fusarium wilt has been the greatest yield-limiting disease of watermelon worldwide. Bruton and Damicone (1999) stated that although Fusarium wilt remains an important disease, it is no longer the greatest constraint to watermelon production in most areas due to the high level of genetic resistance available to farmers. However, the status of Fusarium wilt is dynamic in that new races, which can attack previously resistant cultivars, can develop. If the new stains are ecologically competitive, they can become established and spread throughout the production region. Strains of F. oxysporum are separated into forma specialis and race strictly based on their ability to cause disease on certain hosts and cultivars (Snyder and Hansen, 1940). Propagules of the fungus may be spread by soil, plant debris, and farm implements. Fulton and Winston (1915) first noted that the Fusarium wilt pathogen can be carried on seeds. Several additional reports (Martyn, 1985, Martyn, 1987; Porter, 1928; Taubenhaus, 1935) confirmed that the pathogen can be seed-transmitted. Consequently, infestation of new land may be through infested seed or transplants. Once the pathogen is established in a field, it may survive for 10 years or more in the absence of watermelon (Cirulli, 1972; Ioannou and Poullis, 1991). Fusarium wilt symptoms include damping-off, seedling disease, or wilt during any stage of plant development. The specific symptom that may be exhibited is dependent on environmental conditions, age of plants when infected, and the density and virulence of the pathogen population. Symptoms on mature plants typically appear following fruit-set and may appear as a dull gray-green appearance of the leaves followed by yellowing of the crown foliage, wilting during the heat of the day, and eventual death. Fusarium wilt is considered to be a vine decline disease of watermelon where vine vigor gradually deteriorates (Bruton et al. 1998). As such, Fusarium wilt has symptoms similar to many of the other vine decline diseases of cucurbits. Bruton (1998) noted that Fusarium wilt has likely been one of the most misdiagnosed diseases because of its similarity with other vine decline diseases of watermelon. Differences in isolate virulence have been recognized for many years (McKeen, 1951). Although Crall (1963) reported the existence of two physiologic strains in Florida, he did not attempt to identify them as specific races. Cirulli (1972) also found two strains in Italy and designated them as race 0 and race 1. In 1973, a highly 93

2 aggressive isolate was found in Israel which was designated as race 2 (Netzer and Dishon (1973). Race 2 appears to be fairly widespread in the eastern Mediterranean region including Greece and Turkey (Netzer, 1976), Cyprus (Ioannou and Poullis, 1991), and South Korea (Kwon and Om, 1998). F. oxysporum f. sp. niveum race 2 has been found in several watermelon production areas in Florida, Texas, and Oklahoma (Martyn and Bruton, 1989). More recently, race 2 has been reported in Indiana (Egel et al., 2005) and Maryland and Delaware (Zhou and Everts, 2001). There is no resistance within commercial watermelon cultivars to race 2. In 2006, a new race 3 was described from production fields in Maryland (Zhou et al., 2006). Since race 3 appears to be more aggressive than race 2, it is highly unlikely that resistance will be found within the presently grown commercial cultivars. However, race 1 is still considered to be the predominant race in most watermelon production areas. Races of the pathogen are presently identified using a set of watermelon differentials (Table 1). Race 1 can induce slight to moderate wilt on most cultivars that are classified as resistant to Fusarium wilt, although, Armstrong and Armstrong (1978) concluded that differences between the strains were not sufficient to constitute distinct races. The study by Larkin et al. (1990) illustrates a continuum between race 1 and 2. Furthermore, the distinction between race 0 and race 1 has been questioned (Armstrong and Armstrong, 1978; Larkin et al., 1990; Martyn, 1987; McKeen, 1951; Reid, 1958; Sleeth, 1934). The tests for race differentiation are laborious and often inconclusive. Results may be influenced by age of test plants, environmental factors, inoculum level, and inoculation method (Martyn and McLaughlin, 1983; Shimotsuma et al., 1972). Race identification using host differentials is probably necessary but with severe limitations due to the virulence continuum exhibited in different strains. Table 1. Watermelon genotypes used to differentiate races of Fusarium oxysporum f. sp. niveum a Disease reaction b Genotype Race 0 Race 1 Race 2 Race 3 Sugar Baby S S S S Charleston Gray R S S S Calhoun Gray R R S S PI FR R R R S a Developed from Cirulli (1972), Netzer (1976), Martyn and Netzer (1991), and Zhou et al. (2006). b R = resistant, b S = susceptible. Orton (1913) developed the first wilt-resistant watermelon cultivar by crossing Eden with an African stock citron. Mohammed et al. (1981) suggested that wilt resistance in citron was due to a high level of preformed phenols and phytoalexins following infection. Cultivars are typically described as resistant or susceptible although there is actually a continuum from resistant to susceptible (Elmstrom and Hopkins, 1981; Schenck, 1961). This was further illustrated by using different inoculum concentrations (Martyn and McLaughlin, 1983). Resistance to race 1 of F. oxysporum f. sp. niveum has been attributed to a single dominant gene (Henderson et al., 1970; Netzer and Weintall, 94

3 1980). Netzer and Martyn (1989) reported resistance to race 2 of F. oxysporum f. sp. niveum in the PI Martyn and Netzer (1991) suggested that genes for resistance in PI are not fixed. Zhang and Rhodes (1993) noted that resistance genes to race 2 in PI are epistatic with one or more recessive genes interacting with a dominant gene. Larkin et al.(1993) noted no clear pattern of surface colonization of watermelon roots by F. oxysporum f. sp. niveum with respect to resistant or susceptible cultivars. However, Zhou and Everts (2004) demonstrated that internal stem colonization could be a good predictor of resistance to race 1. Elmstrom and Hopkins (1981) evaluated a number of cultivars and noted moderate to high resistance in several cultivars. Paulus et al. (1976) reported that seedless watermelon cultivars tested under field conditions in California were very susceptible. Currently, most of the seedless cultivars are susceptible to Fusarium wilt. It would appear that many of the present-day triploids have a similar genetic background. With triploids commanding almost 75% of the watermelon market in 2006, Fusarium wilt resistance has again become a major emphasis for seed companies. In retrospect, the watermelon industry in the United States has made drastic changes over the last 30 years. In the late 1970 s, watermelon production consisted of the open-pollinated diploid cultivars such as Black Diamond, Charleston Gray, Jubilee, and others. Seed costs generally ranged between $0.01 and $0.02 for each seed and plants were all direct-seeded. These cultivars tended to have little or no resistance to Fusarium wilt. Crop rotation was the only method of control at the time, and land availability was generally not a constraint. By 1985, hybrid cultivars were beginning to be planted on significant acreages. Many of the diploid hybrids had greatly improved resistance to Fusarium wilt as well as other improved characteristics. Because of seed costs ($ for each seed), hybrid watermelon production was a gradual evolution over several years. In fact, the seed costs were so great that farmers began to use transplants to reduce seedling death in the small-seeded hybrids. Hybrid transplants cost approximately $0.12 each, but allowed for earlier planting dates than for direct-seeding. Transplanting also allowed some farmers to make the fourth of July market which generally received the highest prices. By 1990, the triploid seedless watermelon was gradually being planted. The seed cost was about $0.15 for each seed and they had to be transplanted because of the rigorous germination requirements. The cost of the seedless transplant was about $0.20 for each plant. By 2000, approximately 50% of the watermelon production was seedless triploids. Today, seedless triploids are likely approaching 75% of the US production. As a rule, seedless watermelons have little or no resistance to Fusarium wilt. This likely results from the tetraploids used by those in the seed industry to make seedless triploids. The tetraploids are generally considered to have a genetically similar background and are very susceptible to Fusarium wilt. Consequently, 75% of US watermelon production is at risk to Fusarium wilt. In 2005, seedless triploids were being grafted onto squash or gourd rootstock for control of Fusarium wilt in the United States. Although grafting has been used in Europe for more than 75 years and is very popular in Korea, Japan and some other Asian countries, excessive costs have prevented the practice from being adopted in the US. Taylor et al. (2006) stated that the cost of grafted-transplants would be about $0.75 per plant. At 1500 plants/acre, the additional cost for grafted-transplants would be about $705/acre. There is much work to be done on cultural requirements such as fertility and plant population. In 95

4 fact, it may be possible to reduce grafted plant populations to 1200 or even 1000/acre without affecting yields. The quality and firmness of the fruit from grafted plants make the fruit especially suited for the fresh-cut industry. With approximately 30% of the seedless watermelons being cut and processed for restaurants and fresh-cut produce, it is the fastest growing segment of the watermelon industry. With changing cultural practices, the dominance of seedless watermelon in the market, mandated cessation of methyl bromide use, and diminishing land for crop rotation, Fusarium wilt has re-emerged as a serious yield-limiting disease of watermelon. Clearly, the prevalence of Fusarium wilt coincides with the overall resistance of the watermelon cultivars grown during a specific period of time. New races of the Fusarium wilt pathogen are evolving faster than new resistance genes can be found and incorporated into commercial cultivars. Although currently expensive, grafting holds great promise for watermelon production in the US. In addition to its potential for combating multiple soilborne diseases including Fusarium wilt, grafting provides good yields and excellent fruit quality. Citations Armstrong, G.M., and Armstrong, J.K Formae speciales and races of Fusarium oxysporum causing wilts of the Cucurbitaceae. Phytopathology 68: Bruton, B.D Soilborne diseases in Cucurbitaceae: pathogen virulence and host resistance, p In: J. McCreight, (ed). Cucurbitaceae 98. ASHS Press, Alexandria, Va. Bruton, B.D., and Damicone, J.P Fusarium wilt of watermelon: Impact of race 2 of Fusarium oxysporum f. sp. niveum on watermelon production in Texas and Oklahoma. Subtrop. Plant Sci. 51:4-9. Bruton, B.D., Russo, V.M., Garcia-Jimenez, J., and Miller, M.E Carbohydrate partitioning, cultural practices, and vine decline diseases of cucurbits, p In: J. McCreight, (ed). Cucurbitaceae 98. ASHS Press, Alexandria, Va. Cirulli, M Variation of pathogenicity in Fusarium oxysporum f. sp. niveum and resistance in watermelon cultivars, p In: Actas Congr. Un. Fitopathol. Mediter. Oeiras, 3 rd. Crall, J.M Physiologic specialization in Fusarium oxysporum f. sp. niveum. Phytopathology 53:873 (abstr.). Egel, D. S., Harikrishnan, R., and Martyn, R. D First report of Fusarium oxysporum f. sp. niveum race 2 as causal agent of Fusarium wilt of watermelon in Indiana. Plant Dis. 89:108. Elmstrom, G.W., and Hopkins, D.L Resistance of watermelon cultivars to Fusarium wilt. Plant Dis. 65: Fulton, H.R., and Winston, J.R Watermelon wilt spread by contaminated seed, p In: Biennial Report. N. C. Agri. Exp. Sta. Henderson, W.R., Jenkins, S.F., and Rawlings, J.O The inheritance of Fusarium wilt resistance in watermelon, Citrullus lanatus (Thumb.) Mansf. J. Amer. Soc. Hort. Sci. 95:

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6 Schenck, N.C Resistance of commercial watermelon varieties to Fusarium wilt. Proc. Fla. State Hort. Soc. 74: Shimotsuma, M., Kuc, J., and Jones, C.M The effects of prior inoculations with non-pathogenic fungi on Fusarium wilt of watermelon. HortScience 7: Sleeth, B Fusarium niveum, the cause of watermelon wilt, p In: W. V. Agric. Exp. Stn. Bull Smith, E.F The watermelon disease of the South. Proc. Am. Assoc. Adv. Sci. 43: Snyder, W.C., and Hansen, H.N The species concept in Fusarium. Amer. J. Bot. 27: Taubenhaus, J.J Seeds of watermelons and okra as possible carriers of Fusarium wilt. Phytopathology 25:969. Taylor, M., Bruton, B., Fish, W., and Roberts, W Economics of grafted watermelons as a methyl bromide alternative for disease control and cut-fruit sales, p In: G. J. Holmes, (ed). Cucurbitaceae Universal Printing & Publishing, Raleigh, NC. Zhang, X., and Rhodes, B Inheritance of resistance to races 0, 1, and 2 of Fusarium oxysporum f. sp. niveum in watermelon (Citrullus sp. PI ). Cucurbit Genetics Cooperative16: Zhou, X.G., and Everts, K.L First report of the occurrence of Fusarium oxysporum f. sp. niveum race 2 in commercial watermelon production areas of Maryland and Delaware. Plant Dis. 85:1291. Zhou, X.G., and Everts, K.L Quantification of root and stem colonization of watermelon by Fusarium oxysporum f. sp. niveum and its use in evaluating resistance. Phytopathology 94: Zhou, X.G., Everts, K.L., and Bruton, B.D Race 3, a new race of Fusarium oxysporum f. sp. niveum, the watermelon Fusarium wilt pathogen. Phytopathology. 96(6):S