title: Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5-mediated retrograde pathway in Arabidopsis.
abstract: Photosystem II (PSII) is the most thermolabile photosynthetic complex. Physiological evidence suggests that the small chloroplast heat-shock protein 21 (HSP21) is involved in plant thermotolerance, but the molecular mechanism of its action remains largely unknown. Here, we have provided genetic and biochemical evidence that HSP21 is activated by the GUN5-dependent retrograde signaling pathway, and stabilizes PSII by directly binding to its core subunits such as D1 and D2 proteins under heat stress. We further demonstrate that the constitutive expression of HSP21 sufficiently rescues the thermosensitive stability of PSII and survival defects of the gun5 mutant with dramatically improving granal stacking under heat stress, indicating that HSP21 is a key chaperone protein in maintaining the integrity of the thylakoid membrane system under heat stress. In line with our interpretation based on several lines of in vitro and in vivo protein-interaction evidence that HSP21 interacts with core subunits of PSII, the kinetics of HSP21 binding to the D1 and D2 proteins was determined by performing an analysis of microscale thermophoresis. Considering the major role of HSP21 in protecting the core subunits of PSII from thermal damage, its heat-responsive activation via the heat-shock transcription factor HsfA2 is critical for the survival of plants under heat stress. Our findings reveal an auto-adaptation loop pathway that plant cells optimize particular needs of chloroplasts in stabilizing photosynthetic complexes by relaying the GUN5-dependent plastid signal(s) to activate the heat-responsive expression of HSP21 in the nucleus during adaptation to heat stress in plants.
authors.affiliation: The National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences and National Center of Plant Gene Research (Shanghai), Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.|University of Chinese Academy of Sciences, Beijing, 100049, China.
authors.forename: Si-Ting
authors.initials: ST
authors.lastname: Chen
authors.affiliation: The National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences and National Center of Plant Gene Research (Shanghai), Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.|University of Chinese Academy of Sciences, Beijing, 100049, China.
authors.forename: Ning-Yu
authors.initials: NY
authors.lastname: He
authors.affiliation: The National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences and National Center of Plant Gene Research (Shanghai), Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.|University of Chinese Academy of Sciences, Beijing, 100049, China.
authors.forename: Juan-Hua
authors.initials: JH
authors.lastname: Chen
authors.affiliation: The National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences and National Center of Plant Gene Research (Shanghai), Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, China.
authors.forename: Fang-Qing
authors.initials: FQ
authors.lastname: Guo
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D006360:Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism*; D018869:Heat-Shock Response / Q000235:genetics / Q000502:physiology; D008190:Lyases / Q000235:genetics / Q000378:metabolism; D045332:Photosystem II Protein Complex / Q000235:genetics / Q000378:metabolism*; D030821:Plants, Genetically Modified / Q000235:genetics / Q000378:metabolism; D011485:Protein Binding / Q000235:genetics / Q000502:physiology; D015398:Signal Transduction / Q000235:genetics / Q000502:physiology
chemical_list: D029681:Arabidopsis Proteins; C400143:HSP21 protein, Arabidopsis; D006360:Heat-Shock Proteins; D045332:Photosystem II Protein Complex; D008190:Lyases; C561080:GUN5 protein, Arabidopsis
keywords: Arabidopsis; heat stress; photosynthesis; photosystem II; retrograde signaling; small heat shock protein; thermotolerance