Cyclin-dependent kinase 8 reprograms primary and secondary metabolic pathways at high levels of jasmonate defense
The plant hormone jasmonate (JA) stimulates innate immunity by triggering the degradation of JASMONATE ZIM-DOMAIN (JAZ) proteins, which in turn reconfigure metabolic pathways to produce various defense-related molecules and cellular structures. However, the mechanisms by which JA shifts metabolism to thwart invading organisms remain largely unknown. Here, we employed a JAZ-deficient mutant (jazD) that exhibits heightened chemical defense and strong growth and reproduction inhibition to interrogate this question. Characterization of a genetic suppressor of jazD that rescues its growth phenotype identified a mutation in CYCLIN-DEPENDENT KINASE 8 (CDK8) as the causal mutation. Genetic epistasis analyses revealed that CDK8 in jazD not only contributes to its robust resistance to insect herbivory and necrotrophic pathogens, but also imposes strong inhibitory effects on shoot growth and seed production. Metabolic phenotypes of jazD cdk8 discerned from transcriptomic and metabolomic analyses showed that CDK8 specifically boosts JA-mediated anti-pathogen branch of specialized metabolism. CDK8-mediated resource allocation to defense sinks upon JAZ deficiency was associated with alteration in central carbon metabolism, upregulation of respiration, as well as increased production of proteinogenic amino acids. Our data establish CDK8 as a key regulator of defense-associated primary and secondary metabolism under JA-mediated stress conditions and provide a potential approach to unlink anti-insect defense to growth and reproduction. Overall design: Analysis of Col-0 (wildtype), cdk8-1, jazD, and jazDcdk8-1 (four genotypes), with three biological replicates per genotype - 12 samples in total.