Rice transcription factor OsNAC2 maintains the homeostasis of immune responses to bacterial blight

• Published in: Plant physiology (Bethesda) Vol. 195; no. 1; pp. 785 - 798
• Main Authors: Zhong, Qun, Yu, Jiangtao, Wu, Yiding, Yao, Xuefeng, Mao, Chanjuan, Meng, Xiangzong, Ming, Feng
• Format: Journal Article
• Language: English
• Published: US Oxford University Press 30.04.2024
• Subjects: Disease Resistance - genetics; Gene Expression Regulation, Plant; Homeostasis; Oryza - genetics; Oryza - immunology; Oryza - microbiology; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; Plant Immunity - genetics; Plant Proteins - genetics; Plant Proteins - metabolism; Salicylic Acid - metabolism; Transcription Factors - genetics; Transcription Factors - metabolism; Xanthomonas - pathogenicity; Xanthomonas - physiology
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1093/plphys/kiad683

Abstract Rice (Oryza sativa) bacterial blight, caused by Xanthomonas oryzae pv. Oryzae (Xoo), threatens plant growth and yield. However, the molecular mechanisms underlying rice immunity against Xoo remain elusive. Here, we identified a NAC (NAM-ATAF-CUC) transcription factor OsNAC2 as a negative regulator in the resistance to bacterial blight disease in rice. Constitutive overexpression of OsNAC2 inhibited the expression of salicylic acid (SA) biosynthesis-related genes (i.e. isochorismate synthase 1 (OsICS1), phenylalanine ammonia lyase 3 (OsPAL3), etc.) with adverse impacts on the pathogenesis-related proteins (PRs) responses and compromised blight resistance. Moreover, OsNAC2 interacted with APETALA2/ethylene-responsive element binding protein (AP2/EREBP) transcription factor OsEREBP1 and possibly threatened its protein stability, destroying the favorable interaction of OsEREBP1–Xa21-binding protein OsXb22a in the cytoplasm during Xoo-induced infection. On the contrary, downregulation of OsNAC2 resulted in enhanced resistance to bacterial blight in rice without any growth or yield penalties. Our results demonstrated that OsNAC2 inhibits SA signaling and stably interacted with OsEREBP1 to impair disease resistance. This OsNAC2-OsEREBP1-based homeostatic mechanism provided insights into the competition between rice and bacterial pathogens, and it will be useful to improve the disease resistance of important crops through breeding. A NAC transcription factor inhibits salicylic acid signaling and interacts with a positive regulator of resistance, leading to compromised bacterial blight resistance in rice.