Evaluation of Watermelon and Related Species for Resistance to Race 1W Powdery Mildew

Powdery mildew [Podosphaera xanthii (Castagne) Braun & Shishkoff (syn. Sphaerotheca fuliginea auct. p.p.)] is now a common disease on watermelon [Citrullus lanatus (Thunb.) Matsum. & Nakai] in the United States. In this study, the entire available U.S. Plant Introduction collection of Citrullus Schrad. ex Eckl. & Zeyh. species was evaluated for resistance to P. xanthii race 1W. The collection consists of four Citrullus species and one Praecitrullus Pangalo species [C. lanatus var. citroides (L.H. Bailey) Mansf., C. colocynthis (L.) Schrad.,C. rehmiiDeWinter, and P. fistulosus (Stocks) Pangalo]. Wild-type accessions tended to be more resistant more often than the cultivated species, C. lanatus var. lanatus. None were immune, eight of the 1573 accessions exhibited high levels of resistance, and another 86 demonstrated intermediate resistance. Stem and leaf disease severity were weakly correlated (r = 0.64, P = 0.001). The majority of accessions having resistance were collected in Zimbabwe. Resistance was found in four species. Powdery mildew affects many cucurbit crops worldwide, limiting yield and increasing the need for fungicide application. Except for a few scattered cases of this disease on watermelon fruit (Ivanoff, 1957; McLean, 1970; Robinson and Provvidenti, 1975), powdery mildew has not been a problem for this crop until recently. Since 1996, a new pathotype of powdery mildew has been damaging watermelon crops in the United States (Davis et al., 2001; Keinath, 2000; McGrath, 2001a). Outbreaks of watermelon powdery mildew pathotypes, races 1W and 2W, on watermelon have been confirmed in South Carolina, Georgia, Florida, Oklahoma, Texas, Maryland, New York, Arizona, and California and were determined using melon (Cucumis melo L.) differentials (Davis et al., 2001; McGrath, 2001a). Powdery mildew can decrease plant canopy, reduce yields through decreased fruit size and number of fruit per plant, and reduce fruit quality, flavor, and storage life (Keinath and DuBose, 2004; McGrath and Thomas, 1996). The reduced canopy may also result in sunscald of the remaining fruit, making them unmarketable. Detection of powdery mildew on watermelon can be difficult because the presence of the pathogen is less apparent than on melon. There are at least two symptoms on watermelon: chlorotic spots that occur on leaves accompanied by little or no sporulation and only a small amount of mycelial development, or mycelial and conidial development on either leaf surface with or without the associated chlorotic spots (Davis et al., 2001). Podosphaera xanthii and Golovinomyces cichoracearum (D.C.) V.P. Heluta (formerly Erysiphe cichoracearum D.C.) are the predominant fungi that incite powdery mildew in cucurbits. These organisms differ in virulence against cucurbit species, and in their sensitivity to fungicides (Bertrand, 1991; Epinat et al., 1993; McGrath, 2001a, 2001b). Only one species, P. xanthii, has been reported on watermelon in the United States. Using differential reactions of 10 melon (C. melo) genotypes, seven pathogenically distinct races of P. xanthii can be differentiated (McCreight et al., 1987; Pitrat et al., 1998). More recently, McCreight (2006) reported that there may be as many as 28 races of P. xanthii on melon based on the reported reactions of 30 melon genotypes with as many as eight variants of race 1, and six variants of race 2. The significance of these races defined on melon is not known for watermelon. Resistance of P. xanthii to certain fungicides has been detected, and application of fungicides to undersides of leaves Received for publication 20 Dec. 2006. Accepted for publication 5 Aug. 2007. This work was partially supported by the Cucurbit Crop Germplasm Committee, the National Germplasm System, USDA, ARS, and a fellowship under the OECD Co-operative Research Programme: Biological Resource Management for Sustainable Agriculture Systems. We thank Amy Helms and Anthony Dillard for technical assistance and Robert Jarret for supplying seed from the Citrullus species collection. Some melon differentials were kindly supplied by Dr. Claude Thomas. Corresponding author. E-mail: [email protected]. 790 J. AMER. SOC. HORT. SCI. 132(6):790–795. 2007. is difficult and often requires the use of systemic materials to achieve adequate control of the disease (McGrath and Thomas, 1996). Recent work by Keinath and DuBose (2004) demonstrated effective control of powdery mildew race 2W on watermelon by alternating preventative applications of two fungicides: mancozeb and azoxystrobin. Use of resistant watermelon cultivars in addition to fungicide applications should slow development of P. xanthii resistance to fungicides. We initially screened 100 watermelon plant introduction (PI) accessions for resistance to watermelon race 1W of P. xanthii (Davis et al., 2001). This led to the release of watermelon breeding line (PI 525088-PMR), which has intermediate resistance to race 1W P. xanthii (Davis et al., 2006a). The inheritance of resistance in that line to race 1W is multigenic (Davis et al., 2002) and appears to be independent from resistance to P. xanthii race 2W (Davis et al., 2002, 2006b; Thomas et al., 2005). In the current study, we screened the entire available U.S. Department of Agriculture, Agricultural Research Service (USDAARS), National Genetic Resources Program (NPGS) watermelon accessions for resistance to race 1W to identify additional resistance genes for control of this race. Materials and Methods PLANT MATERIAL. A total of 1573 Citrullus species and tinda (P. fistulosus) accessions from NPGS at the Southern Regional Plant Introduction Station, USDA-ARS, Griffin, GA, were evaluated. The accessions represent 75 countries of origin and five species, belonging to C. lanatus var. lanatus, C. lanatus var. citroides, C. colocynthis, C. rehmii, and P. fistulosus. Ten C. melo differentials were included in all experiments to determine the race of P. xanthii present: ‘Delicious 51’, ‘Edisto 47’, Iran H, MR-1, ‘Nantais Oblong’, PI 124112, PI 414723, ‘PMR 45’, ‘PMR 5’, ‘PMR 6’, WMR 29, and ‘Top Mark’. Differentials were supplied by C. Thomas and M. Pitrat and were included in all studies to verify the Table 1. Ranking of the mean disease severity rating (DSR) from six replicates of Citrullus species and Praecitrullus species PI lines that demonstrated resistance or intermediate resistance to race 1W Podosphaera xanthii. Mean DSR (1–12 scale) Accession Total plant Leaf Cotyledon Stem Species Seed origin Grif 5601 2.0 2.0 2.0 2.0 P India PI 482255 2.5 2.5 2.5 2.5 L Zimbabwe PI 388770 2.7 3.0 2.5 2.5 Cc Morocco PI 482362 2.7 2.5 3.0 2.5 L Zimbabwe PI 381750 2.8 2.5 3.5 2.5 P India PI 459074 2.8 3.0 3.0 2.5 L Botswana PI 386015 3.0 3.0 3.0 3.0 Cc Iran PI 482248 3.0 3.3 3.0 2.7 L Zimbabwe PI 381742 3.2 2.5 4.0 3.0 P India PI 532738 3.2 3.3 3.3 3.0 c Zaire PI 500331 3.3 3.4 3.2 3.4 c Zambia PI 508443 3.3 4.0 3.0 3.0 L South Korea PI 560008 3.3 3.0 4.0 3.0 L Nigeria PI 525082 3.4 4.0 3.5 2.8 Cc Egypt PI 482264 3.4 3.3 3.7 3.3 L Zimbabwe PI 482258 3.5 3.5 3.5 3.5 L Zimbabwe PI 217938 3.6 3.7 3.3 3.7 P Pakistan PI 250145 3.6 4.0 3.3 3.3 P Pakistan PI 482333 3.6 3.3 3.7 3.7 c Zimbabwe PI 526233 3.6 4.0 3.3 3.3 L Zimbabwe PI 482313 3.6 3.8 3.5 3.5 L Zimbabwe PI 482328 3.6 3.5 3.8 3.5 L Zimbabwe PI 500323 3.6 4.0 3.4 3.4 L Zambia PI 505585 3.6 3.8 3.6 3.4 L Zambia PI 169241 3.7 3.0 4.0 4.0 L Turkey PI 179239 3.7 4.0 3.5 3.5 L Turkey PI 179881 3.7 3.0 4.5 3.5 c India PI 179885 3.7 4.0 4.0 3.0 L India PI 184800 3.7 4.0 3.5 3.5 L Nigeria PI 271749 3.7 4.0 3.7 3.3 L Afghanistan PI 296334 3.7 3.3 4.5 3.3 c South Africa PI 381731 3.7 3.5 4.0 3.5 L India PI 386025 3.7 4.5 3.5 3.0 Cc Iran PI 482251 3.7 3.3 3.8 4.0 L Zimbabwe PI 482278 3.7 3.8 4.0 3.3 L Zimbabwe PI 482295 3.7 3.5 4.0 3.5 L Zimbabwe PI 482302 3.7 3.3 3.8 4.0 c Zimbabwe PI 482355 3.7 3.3 4.0 3.8 c Zimbabwe PI 500332 3.7 3.3 4.3 3.5 c Zambia PI 512343 3.7 3.0 5.0 3.0 L Spain PI 525088 3.7 3.3 4.0 3.7 L Egypt PI 482312 3.7 3.8 3.5 3.8 c Zimbabwe PI 482259 3.7 4.0 3.8 3.4 c Zimbabwe PI 482308 3.7 4.0 3.6 3.6 c Zimbabwe PI 482380 3.7 3.6 3.8 3.8 L Zimbabwe PI 500334 3.7 3.8 3.6 3.8 c Zambia PI 270545 3.8 3.5 4.0 3.8 L Sudan PI 482268 3.8 4.3 3.5 3.5 L Zimbabwe Grif 5602 3.8 3.7 4.3 3.3 P India PI 189318 3.8 3.7 3.7 4.0 L Nigeria PI 500302 3.8 3.7 4.0 3.7 c Zambia PI 500308 3.8 3.8 4.0 3.6 c Zambia PI 500342 3.8 3.8 3.6 4.0 L Zambia PI 179875 3.8 4.0 4.3 3.3 P India PI 180275 3.8 3.5 4.5 3.5 P India