STAYGREEN (CsSGR) is a candidate for the anthracnose (Colletotrichum orbiculare) resistance locus cla in Gy14 cucumber

Abstract

Map-based cloning identified a candidate gene for resistance to the anthracnose fungal pathogen Colletotrichum orbiculare in cucumber, which reveals a novel function for the highly conserved STAYGREEN family genes for host disease resistance in plants. Colletotrichum orbiculare is a hemibiotrophic fungal pathogen that causes anthracnose disease in cucumber and other cucurbit crops. No host resistance genes against the anthracnose pathogens have been cloned in crop plants. Here, we reported fine mapping and cloning of a resistance gene to the race 1 anthracnose pathogen in cucumber inbred lines Gy14 and WI 2757. Phenotypic and QTL analysis in multiple populations revealed that a single recessive gene, cla, was underlying anthracnose resistance in both lines, but WI2757 carried an additional minor-effect QTL. Fine mapping using 150 Gy14 × 9930 recombinant inbred lines and 1043 F individuals delimited the cla locus into a 32 kb region in cucumber Chromosome 5 with three predicted genes. Multiple lines of evidence suggested that the cucumber STAYGREEN (CsSGR) gene is a candidate for the anthracnose resistance locus. A single nucleotide mutation in the third exon of CsSGR resulted in the substitution of Glutamine in 9930 to Arginine in Gy14 in CsSGR protein which seems responsible for the differential anthracnose inoculation responses between Gy14 and 9930. Quantitative real-time PCR analysis indicated that CsSGR was significantly upregulated upon anthracnose pathogen inoculation in the susceptible 9930, while its expression was much lower in the resistant Gy14. Investigation of allelic diversities in natural cucumber populations revealed that the resistance allele in almost all improved cultivars or breeding lines of the U.S. origin was derived from PI 197087. This work reveals an unknown function for the highly conserved STAYGREEN (SGR) family genes for host disease resistance in plants.

STAYGREEN, STAY HEALTHY: a loss‐of‐susceptibility mutation in the STAYGREEN gene provides durable, broad‐spectrum disease resistances for over 50 years of US cucumber production

“…c). Similar trends were also observed for CsSGR expression in Gy14 and 9930 after inoculation with the ALS and AR pathogens (Pan et al ., ), supporting a direct link between CsSGR expression and host resistance against these pathogens.…”

“…Our previous work (Pan et al ., ) has shown that CsSGR is a candidate gene for the AR resistance locus cla in PI 197087, suggesting that CsSGR in Gy14 is responsible for simultaneous resistances against DM, ALS and AR. To further confirm this, we conducted local association analysis in natural populations using sequencing data from the 93.7‐kb region and phenotypic data from a subset of lines (presented in Table S4).…”

“…First, loss‐of‐susceptibility R genes are often considered to be nonrace specific. Responses to AR pathogen infection were typical HRs (Pan et al ., ), but Gy14 showed high to moderate resistances to pre‐ and post‐2004 DM strains and two isolates of the P. syringae pv. lachrymans pathogen, respectively (Call et al ., 2012a; Table S5).…”

“…In addition, 41, 50 and 82 cucumber lines were employed for local association analysis using the Ridge Regression algorithm in the R/RRBLUP package (Endelman, 2011). Phenotypic data for these lines to the pre-2004 DM strains, and the AR and ALS inoculation responses, were obtained from historical data (Wehner & Shetty, 1997), and our previous (Pan et al, 2018) and present studies, respectively.…”

“…Nevertheless, dm1 still exhibits moderate resistance to the prevailing post‐2004 DM strains in the USA and sufficient resistance in many other countries. We have recently identified CsSGR as the candidate gene for the AR resistance locus cla in both Gy14 and WI 2757 (Pan et al ., ). Here, we report quantitative trait locus (QTL) mapping and cloning of the dm1 and psl loci in Gy14 and WI2757.…”