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

Abstract

The Gy14 cucumber (Cucumis sativus) is resistant to oomyceteous downy mildew (DM), bacterial angular leaf spot (ALS) and fungal anthracnose (AR) pathogens, but the underlying molecular mechanisms are unknown. Quantitative trait locus (QTL) mapping for the disease resistances in Gy14 and further map-based cloning identified a candidate gene for the resistant loci, which was validated and functionally characterized by spatial-temporal gene expression profiling, allelic diversity and phylogenetic analysis, as well as local association studies. We showed that the triple-disease resistances in Gy14 were controlled by the cucumber STAYGREEN (CsSGR) gene. A single nucleotide polymorphism (SNP) in the coding region resulted in a nonsynonymous amino acid substitution in the CsSGR protein, and thus disease resistance. Genes in the chlorophyll degradation pathway showed differential expression between resistant and susceptible lines in response to pathogen inoculation. The causal SNP was significantly associated with disease resistances in natural and breeding populations. The resistance allele has undergone selection in cucumber breeding. The durable, broad-spectrum disease resistance is caused by a loss-of-susceptibility mutation of CsSGR. Probably, this is achieved through the inhibition of reactive oxygen species over-accumulation and phytotoxic catabolite over-buildup in the chlorophyll degradation pathway. The CsSGR-mediated host resistance represents a novel function of this highly conserved gene in plants.

Identification of novel loci and candidate genes for cucumber downy mildew resistance using GWAS

“…reported that dm5.1, dm5.2, and dm5.3 were major-effect QTLs contributing to DM resistance. Wang et al (2019) identi ed a DM resistance gene STAYGREEN, which also located on Chr5 [12]. Therefore, we proposed that the sites located on Chr5 was the most likely loci on DM resistance.…”

“…Downy mildew was also devastating in cucumber. Many researches on downy mildew in cucumber have been reported [10][11][12]. Zhang et al (2013) constructed the F 2 and F 2:3 population based on the cross of inbred line K8 and K18 and identi ed 5 QTLs (dm1.1, dm5.1, dm5.2, dm5.3 and dm6.1) associated with DM on the Chr1, Chr5 and Chr6, respectively.…”

Characterization, Identification and Expression Profiling of Genome-Wide R-Genes in Melon and Their Putative Roles in Bacterial Fruit Blotch Resistance

“…The clustering of R-genes is an evolutionarily conserved defense mechanism in plants wherein recombination in closely located genes creates new motif combinations, which generates novel resistance speci cities and broadens plant resistance to different diseases [42,64]. R-gene clusters that provide resistance to multiple diseases have been reported for angular leaf spot, downy mildew, and anthracnose diseases in cucumber [65] and for blackleg, sclerotinia stem rot, and clubroot diseases in B. napus [66][67][68] and B. rapa [66]. In melon, a 1 Mb region on chromosome ve contains the highest density of R-genes [69].…”

Gynoecy instability in cucumber (Cucumis sativus L.) is due to unequal crossover at the copy number variation-dependent Femaleness (F) locus

“…The genomic DNA sequence diversity of the 50 kb F locus was examined in 48 re-sequenced cucumbers lines reported previously 86,87 and the three 'gynoecy loss' mutants. SNPs within the target region were called with the BWA-GATK4.0 workflow using 9930 V2.0 as the reference following Wang et al 88 . All detected polymorphisms (SNPs or InDels) in the 30-kb CNV sequence in the 'gynoecy loss' mutants were verified by PCR and Sanger sequencing.…”