Network analyses reveal D clade ethylene response factors as major regulators of jasmonic acid-mediated resistance to early blight disease complex in tomato

Abstract

Resistance mechanisms to early blight disease complex (EBDC) in tomato remain obscure given its polygenic and quantitative nature. We investigated the early defense responses of Heinz 1706 tomato to EBDC using RNA-seq. We observed distinct transcriptional reprofiling upon exposure to two EBDC isolates and the PAMP chitin. Avirulent isolate CS046 (Alternaria alternata) elicited a vigorous defense response in the host, whilst the virulent isolate 1117-1 (Alternariasect.Porri) showed subdued gene expression, suggesting a suppression of defense responses during compatible pathogenesis. We emphasize the specific roles ofETHYLENE RESPONSE FACTORs(ERFs) in defense against EBDC, with a particular focus on the D cladeERFs. Co-expression network analysis revealed the principal genes in early defense responses to EBDC are secondary metabolite biosynthesis genes, transcription factors, and hormone response genes. We constructed a gene regulatory network and predicted novel hub genes as putative global regulators of the defense response, including the D cladeERFs, WRKY, andNACtranscription factors. Our work highlights the failure of virulent EBDC pathogenesis to elicit hormone responses that suppress cell death. Additionally, we found a selective induction for specific ERFs that strongly influence the topology of the EBDC defense transcriptional network.

Alternaria diseases on potato and tomato

“…Transcriptomics studies in the A. solani /potato pathosystem have highlighted the induction of peroxidases, terpene synthases, and JA/ET biosynthesis genes during EBDC infection, but questions remain about how a resistant cultivar is significantly more resistant than a susceptible cultivar (Sajeevan et al., 2023 ). We found that tomatoes treated with avirulent EBDC‐induced expression of D clade ethylene response factors (ERFs) that were highly influential in both co‐expression and gene regulatory networks associated with JA/ET biosynthesis, secondary metabolite biosynthesis and their transporters, detoxification, and calcium signalling (Tominello‐Ramirez et al., 2023 ). Conversely, tomatoes treated with virulent EBDC induced far fewer genes and no clear defence, either SA‐ or JA‐mediated.…”