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

<jats:title>Summary</jats:title><jats:p> <jats:list list-type="bullet"> <jats:list-item><jats:p>The Gy14 cucumber (<jats:italic>Cucumis sativus</jats:italic>) is resistant to oomyceteous downy mildew (<jats:styled-content style="fixed-case">DM</jats:styled-content>), bacterial angular leaf spot (<jats:styled-content style="fixed-case">ALS</jats:styled-content>) and fungal anthracnose (<jats:styled-content style="fixed-case">AR</jats:styled-content>) pathogens, but the underlying molecular mechanisms are unknown.</jats:p></jats:list-item> <jats:list-item><jats:p>Quantitative trait locus (<jats:styled-content style="fixed-case">QTL</jats:styled-content>) 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.</jats:p></jats:list-item> <jats:list-item><jats:p>We showed that the triple‐disease resistances in Gy14 were controlled by the cucumber <jats:italic><jats:styled-content style="fixed-case">STAYGREEN</jats:styled-content></jats:italic> (<jats:italic>Cs<jats:styled-content style="fixed-case">SGR</jats:styled-content></jats:italic>) gene. A single nucleotide polymorphism (<jats:styled-content style="fixed-case">SNP</jats:styled-content>) in the coding region resulted in a nonsynonymous amino acid substitution in the Cs<jats:styled-content style="fixed-case">SGR</jats:styled-content> 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 <jats:styled-content style="fixed-case">SNP</jats:styled-content> was significantly associated with disease resistances in natural and breeding populations. The resistance allele has undergone selection in cucumber breeding.</jats:p></jats:list-item> <jats:list-item><jats:p>The durable, broad‐spectrum disease resistance is caused by a loss‐of‐susceptibility mutation of <jats:italic>Cs<jats:styled-content style="fixed-case">SGR</jats:styled-content></jats:italic>. Probably, this is achieved through the inhibition of reactive oxygen species over‐accumulation and phytotoxic catabolite over‐buildup in the chlorophyll degradation pathway. The <jats:italic>Cs<jats:styled-content style="fixed-case">SGR</jats:styled-content></jats:italic>‐mediated host resistance represents a novel function of this highly conserved gene in plants.</jats:p></jats:list-item> </jats:list> </jats:p>