GCN5-related histone acetyltransferase HOOKLESS2 regulates fungal resistance and growth in tomato

The functions of histone acetyltransferases (HATs) in the genetic control of crop traits and the underlying mechanisms are poorly understood. We studied the function of tomato HOOKLESS2 (SlHLS2), a member of the GCN5 family of HATs, through genetic, molecular and genomic approaches. Tomato hls2 mutants generated through CRISPR-cas9 gene editing show enhanced susceptibility to fungal infection, accelerated dark-induced senescence, grossly altered plant architecture, and loss of fertility accompanied by high levels of auxin accumulation. Components of the basal and induced transcriptome underlying the extensive phenotypic impact of HLS2 were uncovered. HLS2-dependent differentially expressed genes were enriched for genes implicated in photosynthesis, protein ubiquitination, oxylipin biosynthesis, autophagy, and response to biotic stimuli. In particular, induced expressions of the BTB/POZ and TAZ domain-containing protein gene (SlBT1), AUTOPHAGY-RELATED PROTEIN 11, ACYLSUGAR ACYLTRANSFERASE 3 (ASAT3), and multiple jasmonate biosynthesis genes require functional HLS2. SlHLS2 associates with the SlBT1 promoter, and histone acetylation at the chromatin of SlBT1 was reduced in the Slhls2 mutant suggesting direct regulation of SlBTB1 by HLS2. SlBTB1 is an adapter of an E3 ubiquitin-protein ligase complex (CUL3-RBX1-BTB), which mediates ubiquitination and proteasomal degradation of proteins. HLS2 is degraded after fungal inoculation, which is stabilized by inhibition of the 26S proteasome. Overall, tomato HLS2 functions in pathogen responses, plant architecture, and fertility.