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

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.