title: Opposing Effects on Two Phases of Defense Responses from Concerted Actions of HEAT SHOCK COGNATE70 and BONZAI1 in Arabidopsis.
abstract: The plant immune system consists of multiple layers of responses targeting various phases of pathogen infection. Here, we provide evidence showing that two responses, one controlling stomatal closure and the other mediated by intracellular receptor proteins, can be regulated by the same proteins but in an antagonistic manner. The HEAT SHOCK COGNATE70 (HSC70), while previously known as a negative regulator of stomatal closure, is a positive regulator of immune responses mediated by the immune receptor protein SUPPRESSOR OF NPR1-1, CONSTITUTIVE1 (SNC1) as well as basal defense responses. In contrast to HSC70, a calcium-binding protein, BONZAI1 (BON1), promotes abscisic acid- and pathogen-triggered stomatal closure in addition to and independent of its previously known negative role in SNC1 regulation. BON1 likely regulates stomatal closure through activating SUPPESSOR OF THE G2 ALLELE OF SKP1 VARIANT B and inhibiting HSC70. New functions of BON1 and HSC70 identified in this study thus reveal opposite effects of each of them on immunity. The opposing roles of these regulators at different phases of plant immune responses exemplify the complexity in immunity regulation and suggest that immune receptors may guard positive regulators functioning at stomatal closure control.
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Mingyue
authors.identifier: http://orcid.org/0000-0001-8855-6617
authors.initials: M
authors.lastname: Gou
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Zemin
authors.initials: Z
authors.lastname: Zhang
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Ning
authors.identifier: http://orcid.org/0000-0002-3974-6921
authors.initials: N
authors.lastname: Zhang
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Quansheng
authors.identifier: http://orcid.org/0000-0001-5249-8427
authors.initials: Q
authors.lastname: Huang
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Jacqueline
authors.initials: J
authors.lastname: Monaghan
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Huijun
authors.initials: H
authors.lastname: Yang
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Zhenying
authors.identifier: http://orcid.org/0000-0002-8441-2162
authors.initials: Z
authors.lastname: Shi
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.).
authors.forename: Cyril
authors.initials: C
authors.lastname: Zipfel
authors.affiliation: Plant Biology Section, School of Integrated Plant Science, Cornell University, Ithaca, New York 14853 (M.G., Z.Z., N.Z., Q.H., H.Y., Z.S., J.H.);State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, College of Agriculture, South China Agricultural University, Guangzhou 510642, China (Z.Z.);State Key Laboratory of Rice Biology, Institute of Nuclear Agricultural Sciences, Zhejiang University, Hangzhou 310029, China (N.Z.);Institute of Nuclear and Biological Technology, Xinjiang Academy of Agricultural Sciences, Urumqi 830091, China (Q.H.);The Sainsbury Laboratory, Norwich Research Park, Norwich NR4 7UH, United Kingdom (J.M., C.Z.); andShanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China (Z.S.) jh299@cornell.edu.
authors.forename: Jian
authors.identifier: http://orcid.org/0000-0002-3777-3344
authors.initials: J
authors.lastname: Hua
mesh_terms: D000040:Abscisic Acid / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics* / Q000276:immunology / Q000502:physiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002135:Calcium-Binding Proteins / Q000235:genetics / Q000378:metabolism; D002352:Carrier Proteins / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism; D050883:HSC70 Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism*; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D010641:Phenotype; D010935:Plant Diseases / Q000276:immunology*; D057865:Plant Immunity; D018515:Plant Leaves / Q000235:genetics / Q000276:immunology / Q000502:physiology; D054046:Plant Stomata / Q000235:genetics / Q000276:immunology / Q000502:physiology; D044224:Pseudomonas syringae / Q000502:physiology; D036226:Seedlings / Q000235:genetics / Q000276:immunology / Q000502:physiology; D020798:Two-Hybrid System Techniques
chemical_list: D029681:Arabidopsis Proteins; C436490:BON1 protein, Arabidopsis; D002135:Calcium-Binding Proteins; D002352:Carrier Proteins; D018797:Cell Cycle Proteins; D050883:HSC70 Heat-Shock Proteins; D008565:Membrane Proteins; C452192:SGT1b protein, Arabidopsis; C482739:SNC1 protein, Arabidopsis; D000040:Abscisic Acid