title: The Arabidopsis transcription factor BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 is a direct substrate of MITOGEN-ACTIVATED PROTEIN KINASE6 and regulates immunity.
abstract: Pathogen-associated molecular patterns (PAMPs) are recognized by plant pattern recognition receptors to activate PAMP-triggered immunity (PTI). Mitogen-activated protein kinases (MAPKs), as well as other cytoplasmic kinases, integrate upstream immune signals and, in turn, dissect PTI signaling via different substrates to regulate defense responses. However, only a few direct substrates of these signaling kinases have been identified. Here, we show that PAMP perception enhances phosphorylation of BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 (BES1), a transcription factor involved in brassinosteroid (BR) signaling pathway, through pathogen-induced MAPKs in Arabidopsis (Arabidopsis thaliana). BES1 interacts with MITOGEN-ACTIVATED PROTEIN KINASE6 (MPK6) and is phosphorylated by MPK6. bes1 loss-of-function mutants display compromised resistance to bacterial pathogen Pseudomonas syringae pv tomato DC3000. BES1 S286A/S137A double mutation (BES1(SSAA)) impairs PAMP-induced phosphorylation and fails to restore bacterial resistance in bes1 mutant, indicating a positive role of BES1 phosphorylation in plant immunity. BES1 is phosphorylated by glycogen synthase kinase3 (GSK3)-like kinase BR-insensitive2 (BIN2), a negative regulator of BR signaling. BR perception inhibits BIN2 activity, allowing dephosphorylation of BES1 to regulate plant development. However, BES1(SSAA) does not affect BR-mediated plant growth, suggesting differential residue requirements for the modulation of BES1 phosphorylation in PTI and BR signaling. Our study identifies BES1 as a unique direct substrate of MPK6 in PTI signaling. This finding reveals MAPK-mediated BES1 phosphorylation as another BES1 modulation mechanism in plant cell signaling, in addition to GSK3-like kinase-mediated BES1 phosphorylation and F box protein-mediated BES1 degradation.
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.).
authors.forename: Sining
authors.initials: S
authors.lastname: Kang
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.).
authors.forename: Fan
authors.initials: F
authors.lastname: Yang
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.).
authors.forename: Lin
authors.initials: L
authors.lastname: Li
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.).
authors.forename: Huamin
authors.initials: H
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.).
authors.forename: She
authors.initials: S
authors.lastname: Chen
authors.affiliation: State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China (S.K., F.Y., J.Z.);University of Chinese Academy of Sciences, Beijing 100049, China (F.Y.); National Institute of Biological Sciences, Zhongguancun Life Science Park, Beijing 102206, China (L.L., S.C.); andState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China (H.C.) zhangjie@im.ac.cn.
authors.forename: Jie
authors.initials: J
authors.lastname: Zhang
mesh_terms: D017360:Arabidopsis / Q000201:enzymology* / Q000276:immunology* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000378:metabolism*; D060406:Brassinosteroids / Q000494:pharmacology; D004268:DNA-Binding Proteins; D060467:Disease Resistance / Q000276:immunology; D004789:Enzyme Activation / Q000187:drug effects; D005408:Flagellin / Q000378:metabolism; D018546:Hypocotyl / Q000187:drug effects / Q000254:growth & development; D020928:Mitogen-Activated Protein Kinases / Q000378:metabolism*; D009687:Nuclear Proteins / Q000378:metabolism*; D010766:Phosphorylation / Q000187:drug effects; D010768:Phosphoserine / Q000378:metabolism; D010935:Plant Diseases / Q000276:immunology / Q000382:microbiology; D057865:Plant Immunity / Q000187:drug effects; D018517:Plant Roots / Q000187:drug effects / Q000254:growth & development; D011485:Protein Binding / Q000187:drug effects; D044224:Pseudomonas syringae / Q000187:drug effects; D013379:Substrate Specificity / Q000187:drug effects
chemical_list: D029681:Arabidopsis Proteins; C456160:BES1 protein, Arabidopsis; D060406:Brassinosteroids; D004268:DNA-Binding Proteins; D009687:Nuclear Proteins; D005408:Flagellin; D010768:Phosphoserine; C436293:MPK6 protein, Arabidopsis; D020928:Mitogen-Activated Protein Kinases