Photosystem Perturbation by <i>Staygreen</i> Mutations Confers Allele‐Dependent Defences Against Infections of Pathogens With Different Lifestyles and Abiotic Stress Tolerance

The staygreen (SGR) gene encodes the magnesium dechelatase that plays an important regulatory role during chlorophyll degradation. Our previous work revealed a nonsynonymous SNP (A323G) inside cucumber CsSGR that is responsible for multiple disease resistance (MDR), but the underlying mechanism is unknown. Here we report the development, phenotypic, genetic, or transcriptomic characterisation of near-isogenic lines for the A323G locus and knock-out mutants of CsSGR (SGRΔ37 with 37-bp deletion) in response to biotic/abiotic stresses. Both SNP and SGRΔ37 mutants show enhanced MDR against infection of five pathogens with different lifestyles, as well as low-temperature tolerance than the wildtype, and SGRΔ37 is a stronger allele with higher resistance/tolerance than the A323G allele. Physical interactions of CsSGR with itself and other chlorophyll catabolic enzymes (CCEs), light-harvesting chlorophyll a/b-binding1 proteins (LHCB1s), and the chlorophyll homoeostasis regulator CsBCM are significantly reduced or abolished in A323G and SGRΔ37 mutants, respectively. Comparative transcriptome analyses revealed a complex regulatory network in which both passive and active defences contribute to Cssgr-conferred MDR. The loss-of-susceptibility CsSGR mutations downregulate expression of chlorophyll catabolic genes, slow down chlorophyll degradation, and delay pathogenesis-induced senescence, thus providing passive defence. The active defence involves SA and/or JA biosynthesis/signalling pathways, which are likely triggered by ROS-mediated retrograde signalling due to perturbation of the photosynthetic electron transport chain. We propose that CsSGR is a target of choice for gene editing to develop mutant alleles for enhanced MDR. Further, mutations of genes involving chlorophyll metabolism, photosystems, or chloroplast development could be a potential source of MDR for plant breeding.