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

Authors: Jaiswal, Namrata; LIAO, CHAO-JAN - Purdue University; HEWAVIDANA, AYOMI INDIKA - Purdue University; MENGISTE, TESFAYE - Purdue University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/5/2025
Publication Date: 2/28/2025
Citation: Jaiswal, N., Liao, C., Hewavidana, A., Mengiste, T. 2025. GCN5-related histone acetyltransferase HOOKLESS2 regulates fungal resistance and growth in tomato. New Phytologist. https://doi.org/10.1111/nph.70025.
DOI: https://doi.org/10.1111/nph.70025

Interpretive Summary: Fungal pathogens present the most significant threats to crop productivity. However, molecular mechanisms of crop resistance to pathogens, especially those with a broad host range, have not been well established. Botrytis cinerea is one of the most important fungal pathogens with a broad host range, infecting tomato worldwide. Histone acetylation (HAc) plays a critical role in the control of gene expression on pathogen attack. The biological functions of HAc and the underlying molecular and biochemical mechanisms are poorly understood in plants. In this paper gene editing was used to turn off a gene in tomato plants called HOOKLESS2 (HLS2) which regulates HAc. We observed that when HLS2 was inactivated, tomatoes became much more susceptible to Botrytis. This work demonstrates that the HAc process plays a very significant role in resistance to Botrytis and likely other fungi and will guide future research to improve disease resistance in plants.

Technical Abstract: The role of histone acetyl transferases (HATs) in the genetic control of crop traits and the underlying mechanisms are poorly understood. We studied the functions of tomato HOOKLESS2 (SlHLS2) which is a member of GCN5 family of HATs. Tomato SlHLS2 was induced by pathogen infection and the plant hormones ethylene, auxin, and abscisic acid. Significantly, tomato Slhls2 mutants generated through CRISPR-cas9 gene editing show enhanced susceptibility to fungal pathogens, accelerated dark induced senescence, significantly altered plant architecture, and complete loss of fertility. The basal and induced transcriptome underlying the extensive impact of HLS2 was uncovered. HLS2 dependent DEGs were enriched for genes implicated in photosynthesis, protein ubiquitination, oxylipin biosynthesis, autophagy and response to biotic stimuli. SlHLS2 associates with SlBTI promoter; and histone acetylation at chromatin of SlBT1 was reduced in Slhls2 mutant suggesting direct regulation of SlBTB1 by HLS2. SlBTB1 is a substrate-specific 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 that is stabilized by inhibition of the 26S proteosome. Overall, tomato HLS2 has a pervasive function in pathogen responses, plant architecture, and fertility.