Two interacting ethylene response factors negatively regulate peach resistance to Lasiodiplodia theobromae

• Published in: Plant physiology (Bethesda) Vol. 192; no. 4; pp. 3134 - 3151
• Main Authors: Zhang, Dongmei, Zhu, Kaijie, Shen, Xingyi, Meng, Jian, Huang, Xue, Tan, Yuqi, Cardinale, Francesca, Liu, Jihong, Li, Guohuai, Liu, Junwei
• Format: Journal Article
• Language: English
• Published: US Oxford University Press 03.08.2023
• Subjects: Ethylenes - metabolism; Plants; Prunus persica - genetics; Prunus persica - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1093/plphys/kiad279

Abstract Gummosis is 1 of the most common and destructive diseases threatening global peach (Prunus persica) production. Our previous studies have revealed that ethylene and methyl jasmonate enhance peach susceptibility to Lasiodiplodia theobromae, a virulent pathogen inducing gummosis; however, the underlying molecular mechanisms remain obscure. Here, 2 ethylene response factors (ERFs), PpERF98 and PpERF1, were identified as negative regulators in peach response to L. theobromae infection. Expression of 2 putative paralogs, PpERF98-1/2, was dramatically induced by ethylene and L. theobromae treatments and accumulated highly in the gummosis-sensitive cultivar. Silencing of PpERF98-1/2 increased salicylic acid (SA) content and pathogenesis-related genes PpPR1 and PpPR2 transcripts, conferring peach resistance to L. theobromae, whereas peach and tomato (Solanum lycopersicum) plants overexpressing either of PpERF98-1/2 showed opposite changes. Also, jasmonic acid markedly accumulated in PpERF98-1/2-silenced plants, but reduction in PpPR3, PpPR4, and PpCHI (Chitinase) transcripts indicated a blocked signaling pathway. PpERF98-1 and 2 were further demonstrated to directly bind the promoters of 2 putative paralogous PpERF1 genes and to activate the ERF branch of the jasmonate/ethylene signaling pathway, thus attenuating SA-dependent defenses. The lesion phenotypes of peach seedlings overexpressing PpERF1-1/2 and PpERF98-1/2 were similar. Furthermore, PpERF98-1/2 formed homodimers/heterodimers and interacted with the 2 PpERF1 proteins to amplify the jasmonate/ethylene signaling pathway, as larger lesions were observed in peach plants cooverexpressing PpERF98 with PpERF1 relative to individual PpERF98 overexpression. Overall, our work deciphers an important regulatory network of ethylene-mediated peach susceptibility to L. theobromae based on a PpERF98-PpERF1 transcriptional cascade, which could be utilized as a potential target for genetic engineering to augment protection against L. theobromae-mediated diseases in crops and trees. Two interacting ethylene response factors (ERFs) negatively regulate resistance by activating the ERF branch of jasmonate/ethylene signaling in Lasiodiplodia theobromae-induced peach gummosis.