[No authors listed]
Photosystem II (PSII) is the most thermolabile photosynthetic complex. Physiological evidence suggests that the small chloroplast heat-shock protein 21 (HSP 21) is involved in plant thermotolerance but the molecular mechanism of its action remains largely unknown. Here, we have provided genetic and biochemical evidence that HSP 21 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 thermo-sensitive stability of PSII and survival defects of the gun5 mutant with dramatically improving granal stacking under heat stress, indicating that HSP21 is a master chaperone protein in maintaining the integrity of 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 analysis of microscale thermophoresis. Considering a major role of HSP21 in protecting the core subunits of PSII from thermal damages, 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. This article is protected by copyright. All rights reserved.
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