Cucurbit powdery mildew of melon incited by Podosphaera xanthii: global and western U.S. perspectives.

Cucurbit powdery mildew (CPM) is a major problem of melon (Cucumis melo L.) production worldwide, that is mostly caused by two fungi: Podosphaera xanthii (Px; formerly Sphaerotheca fuliginea) and Golovinomyces cichoracearum (DC) V.P. Heluta (Gc; formerly Erysiphe cichoracearum). The two species may co-infect in some areas of northern Europe, but Px dominates in warmer climates around the world. Forty-five races of Px have been reported on melon based on sets of race differentials that range in number from as few as two to as many as 28. The CPM research community and seed industry are undertaking steps to define uniform sets of CPM race differentials and objective criteria for race nomenclature and designations. Breeders and pathologists must also consider another aspect of CPM that stems from its obligate parasitic nature: race stability as defined by a given set of CPM race differentials. This review summarizes the reported races of Px largely from the published literature. It also presents annual profiles from 2002 through 2011 of Px populations in the Central and Imperial valleys of California, and Yuma, Arizona. It is suggested that a large fraction of the races are not relevant to most Px resistance breeding, which will be done on a regional basis for subsets of races. INTRODUCTION Two fungi are commonly credited for inciting cucurbit powdery mildew (CPM) worldwide: Podosphaera xanthii (Px; formerly Sphaerotheca fuliginea) and Golovinomyces cichoracearum (DC) V.P. Heluta (Ec; formerly Erysiphe cichoracearum) (Shishkoff, 2000). Px predominates in warmer areas while Ec does so in cooler areas, and mixed infections (Px and Gc) have been found in Europe (Bertrand, 1991; Křístková, et al., 2009). The two CPM pathogens were confounded for many years as Gc (McCreight, 2004), but Px appears to be the predominant pathogen in major melon production areas. The increased numbers of reported Px races has stimulated concern over the future of breeding melons resistant to Px, in particular the need for a concise and objective system for Px race denomination and designation (see Lebeda, et al., 2012).We review here the gradual increase in the complexity of Pxand Gc-melon interactions over 87 years, expressed as pathogenic races, which has recently escalated (Fig. 1). REPORTED PATHOLOGICAL RACES Imperial Valley, California melon growers suffered losses to Px starting in 1925. Scientific breeding for resistance to Px was initiated in 1928 upon discovery of variation for reaction to Px in germplasm from India and resulted in the release of ‘PMR 45’ in 1934 (Jagger and Scott, 1937). Pathogenic race variation within Px was first observed in 1937 when ‘PMR 45’ was observed to be widely infected in Imperial Valley (Jagger, et al., 1938; Fig. 1). Resistance to this new form of Px, designated race 2, was quickly found and resulted in the release of ‘PMR 5’ in 1942 (Pryor, et al., 1946). A third Px race on melons was observed by C.E. Thomas in the lower Rio Grande Valley of Texas in 1976 (Thomas, 1978). Race 3, as this new strain became known, did not become widespread in Texas or the U.S, but was later reported in the Punjab of India (Kaur and Jhooty, 1986) and widespread in Israel (Cohen, et al., 1996). PI 414723 and WMR 29 revealed variation within Px race 2: 2US and 2F (France) in 1986 (McCreight, et al., 1987). Four Px races were known on melon in 1986 (Fig. 1). By 1998, seven Px races, including 2US and 2F, were reported (Pitrat, et al., 1998). Race 0 revealed Px-resistance factors in ‘Védrantais’ and ‘Top Mark’ that had been regarded as universal Px susceptible genotypes (Bardin, et al., 1997). Races 4 and 5 were observed at about the same time (1997–1998) in France (M. Pitrat, pers. commun.) and Czech Republic (Krístková and Lebeda, 1999) and later in Israel (Cohen, et al., 2004). The number of reported Px races increased dramatically from this time (Fig. 1). Four new races (N1, N2, N3, N4) were reported from Japan in 2000 (Hosoya, et al., 2000). Two variants each of Px races 2 and 3 were reported in 2002 (Cohen, et al., 2002). Bertrand (2002) reported race 6 using AR Hale’s Best Jumbo. Race S was first observed in Imperial Valley in 2003 (McCreight, et al., 2005). Races F, G, H were found in Czech (Lebeda and Sedláková, 2006). Then, there were 20 Px races (Fig. 1). Px race SD was isolated from Imperial Valley in 2004 or 2005 (Coffey, et al., 2006), and shortly afterwards was present in a greenhouse at Salinas (J.D. McCreight, unpub. data). Races 3.5 and P6 were reported in 2005 (M. Pitrat, pers. commun.). Race 4.5 was reported in 2008 Pitrat and Besombes, 2008 Comparative studies of reported Px resistance sources identified in California, Japan, and Spain differentiated isolates/populations of Px race 1 (eight variants; seven new) and race 2 (six variants; two new) populations in these countries (McCreight, 2006). A unique race, pxCh 1 was reported in China in 2010 (Liu, et al., 2010). Twelve new Px races were isolated in 2010 in Czech Republic (Lebeda, et al., 2012). Forty-five Px and 13 Gc races have thus been reported to date on melon (Table 1). This total for Px ignores the variation in Px at the pathotype level, e.g, isolates of races S and SD vary in their ability to infect watermelon Citrullus lanatus (Coffey, et al., 2006). RACE STABILITY IN CALIFORNIA AND ARIZONA Px Race 2 was the presumed race in California after many years of the deployment of Px race 2-resistant cultivars. Px race 1 was, however, detected at the Univ. Calif. (UC), Desert Crops Res. and Ext. Ctr. (DREC), Holtville, CA 92243 in the Imperial Valley six of 10 yrs from 2002 through 2011; Px race S was present three years, and race 2 was present one year (Table 2). In Yuma, Arizona, Px race 1 was present in Spring 2003, but Px race S was isolated from that field via single spore transfer and was consistently present in four subsequent Spring tests (Table 2). Px race 1 was detected in four, Fall field tests in Yuma. Px race 1 was present at UC West Side Res. and Ext. Ctr., Five Points, CA 93624-0158 in the San Joaquin Valley in 2003 (ca. 460 km north of DREC); Px race S was found there in 2007. Px race S was detected at two sites in 2011 in the Davis– Woodland area, which is ca. 340 km north of Five Points. Px race S is becoming more widespread throughout the Central Valley of California. It remains to be seen whether the Px populations will be consistently race S, or vary annually, like in Imperial Valley.