The MAPK-Alfin-like 7 module negatively regulates ROS scavenging genes to promote NLR-mediated immunity

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 120; no. 3; p. e2214750120
• Main Authors: Zhang, Dingliang, Gao, Zongyu, Zhang, He, Yang, Yizhou, Yang, Xinxin, Zhao, Xiaofei, Guo, Hailong, Nagalakshmi, Ugrappa, Li, Dawei, Dinesh-Kumar, Savithramma P, Zhang, Yongliang
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 17.01.2023
• Subjects: Binding; Biological Sciences; Deoxyribonucleic acid; Disease resistance; DNA; Genes; Immune response; Immune system; Immunity; Interleukin 1; Kinases; Leucine; Leucine - metabolism; MAP kinase; Modules; Nicotiana - metabolism; Nucleotides; Nucleotides - metabolism; Plant Immunity; Plant Proteins - genetics; Plant Proteins - metabolism; Protein Domains; Protein kinase; Proteins; Reactive oxygen species; Reactive Oxygen Species - metabolism; Receptors; Repressors; Salicylic acid; Scavenging; Tobacco; Transcription factors; Transcription Factors - metabolism; Viruses; Alfin-like 7; TMV; N NLR immune receptor; transcriptional repressor; MAPKs
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2214750120

Nucleotide-binding leucine-rich repeat (NLR) receptor-mediated immunity includes rapid production of reactive oxygen species (ROS) and transcriptional reprogramming, which is controlled by transcription factors (TFs). Although some TFs have been reported to participate in NLR-mediated immune response, most TFs are transcriptional activators, and whether and how transcriptional repressors regulate NLR-mediated plant defenses remains largely unknown. Here, we show that the Alfin-like 7 (AL7) interacts with N NLR and functions as a transcriptional repressor. Knockdown and knockout of compromise -mediated resistance against tobacco mosaic virus, whereas overexpression enhances defense, indicating a positive regulatory role for AL7 in immunity. AL7 binds to the promoters of ROS scavenging genes to inhibit their transcription during immune responses. Mitogen-activated protein kinases (MAPKs), salicylic acid-induced protein kinase (SIPK), and wound-induced protein kinase (WIPK) directly interact with and phosphorylate AL7, which impairs the AL7-N interaction and enhances its DNA binding activity, which promotes ROS accumulation and enables immune activation. In addition to N, AL7 is also required for the function of other Toll interleukin 1 receptor/nucleotide-binding/leucine-rich repeats (TNLs) including Roq1 and RRS1-R/RPS4. Our findings reveal a hitherto unknown MAPK-AL7 module that negatively regulates ROS scavenging genes to promote NLR-mediated immunity.