Quality Control of Photosystem II: The Mechanisms for Avoidance and Tolerance of Light and Heat Stresses are Closely Linked to Membrane Fluidity of the Thylakoids

Yamamoto, Yasutake

doi:10.3389/fpls.2016.01136

Cited by 117 publications

(99 citation statements)

References 113 publications

(166 reference statements)

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“…Several studies suggest that thylakoids require a particularly high level of fluidity regulation for the proper functioning of the embedded proteins, which occupy about 70% of the membranes (Kirchhoff et al ., ; Dormann and Holzl, ; Yamamoto, ). As these membranes provide the matrix for the photosynthetic machinery, the fluidity regulation processes we highlight in this study are likely essential mechanisms for survival and competitiveness of a cyanobacterial strain at different temperatures.…”

Section: Resultsmentioning

confidence: 99%

“…PCC 6803 and Synechococcus sp. PCC 7942, a number of mutant studies have demonstrated that PG is physiologically essential and is notably involved in the activity of both photosystems, influencing the dimerization and reactivation of core complexes (Sakurai et al, 2003;Bogos et al, 2010;Yamamoto, 2016). X-ray crystallographic analysis of photosystem II at 1.9 Å resolution has identified 5 PG molecules bound to photosystem II, directly connected to the D1 protein and plastoquinone Q B (Itoh et al, 2012;Mizusawa and Wada, 2012).…”

Section: Cold-induced Desaturations Of Acyl Chains In Synechococcus Smentioning

confidence: 99%

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Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus

Pittera

Jouhet

Breton

et al. 2017

Environmental Microbiology

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The marine cyanobacteria of the genus Synechococcus are important primary producers, displaying a wide latitudinal distribution that is underpinned by diversification into temperature ecotypes. The physiological basis underlying these ecotypes is poorly known. In many organisms, regulation of membrane fluidity is crucial for acclimating to variations in temperature. Here, we reveal the detailed composition of the membrane lipidome of the model strain Synechococcus sp. WH7803 and its response to temperature variation. Unlike freshwater strains, membranes are almost devoid of C18, mainly containing C14 and C16 chains with no more than two unsaturations. In response to cold, we observed a rarely observed process of acyl chain shortening that likely induces membrane thinning, along with specific desaturation activities. Both of these mechanisms likely regulate membrane fluidity, facilitating the maintenance of efficient photosynthetic activity. A comprehensive examination of 53 Synechococcus genomes revealed clade-specific gene sets regulating membrane lipids. In particular, the genes encoding desaturase enzymes, which is a key to the temperature stress response, appeared to be temperature ecotype-specific, with some of them originating from lateral transfers. Our study suggests that regulation of membrane fluidity has been among the important adaptation processes for the colonization of different thermal niches by marine Synechococcus.

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Section: Resultsmentioning

confidence: 99%

Section: Cold-induced Desaturations Of Acyl Chains In Synechococcus Smentioning

confidence: 99%

Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus

Pittera

Jouhet

Breton

et al. 2017

Environmental Microbiology

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“…The structure of the thylakoid membranes is dependent on lipids located either at the membrane‐exposed surface of protein complexes or at well‐defined positions of the proteins (Yamamoto, ). Heat stress‐induced inactivation of photosystem II is likely to be affected by the alterations in the fluidity of the thylakoid membranes (Yamamoto, ). Based on the results presented in this study, our findings support a major role of HSP21 in stabilizing the thylakoid membranes by directly interacting with the core subunits of PSII, although we cannot rule out the possibility that HSP21 may function in protecting the fluidity of the thylakoid membranes under heat stress.…”

Section: Discussionmentioning

confidence: 98%

“…It has been proposed that chemical and biological reactions occurring in the thylakoids can be regulated by membrane fluidity (Mizusawa and Wada, ; Yamamoto, ). The structure of the thylakoid membranes is dependent on lipids located either at the membrane‐exposed surface of protein complexes or at well‐defined positions of the proteins (Yamamoto, ). Heat stress‐induced inactivation of photosystem II is likely to be affected by the alterations in the fluidity of the thylakoid membranes (Yamamoto, ).…”

Section: Discussionmentioning

confidence: 99%

Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5‐mediated retrograde pathway in Arabidopsis

Chen

et al. 2017

The Plant Journal

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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.

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“…Combination of high light and moderate heat stress negatively affects PSII, with additive or synergistic effects on thylakoid membrane fluidity, lipid peroxidation, and oxidative damage (Quiles, 2006;Yamamoto, 2016). Moreover, chloroplast signaling is involved in heat stress responses (Dickinson et al, 2017).…”

Section: Integrative Effects Of Stress Hubs and Cell Surveillance Smentioning

confidence: 99%

Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

Bigot

Buges

Gilly

et al. 2018

Global Change Biology

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Climate change reshapes the physiology and development of organisms through phenotypic plasticity, epigenetic modifications, and genetic adaptation. Under evolutionary pressures of the sessile lifestyle, plants possess efficient systems of phenotypic plasticity and acclimation to environmental conditions. Molecular analysis, especially through omics approaches, of these primary lines of environmental adjustment in the context of climate change has revealed the underlying biochemical and physiological mechanisms, thus characterizing the links between phenotypic plasticity and climate change responses. The efficiency of adaptive plasticity under climate change indeed depends on the realization of such biochemical and physiological mechanisms, but the importance of sensing and signaling mechanisms that can integrate perception of environmental cues and transduction into physiological responses is often overlooked. Recent progress opens the possibility of considering plant phenotypic plasticity and responses to climate change through the perspective of environmental sensing and signaling. This review aims to analyze present knowledge on plant sensing and signaling mechanisms and discuss how their structural and functional characteristics lead to resilience or hypersensitivity under conditions of climate change. Plant cells are endowed with arrays of environmental and stress sensors and with internal signals that act as molecular integrators of the multiple constraints of climate change, thus giving rise to potential mechanisms of climate change sensing. Moreover, mechanisms of stress-related information propagation lead to stress memory and acquired stress tolerance that could withstand different scenarios of modifications of stress frequency and intensity. However, optimal functioning of existing sensors, optimal integration of additive constraints and signals, or memory processes can be hampered by conflicting interferences between novel combinations and novel changes in intensity and duration of climate change-related factors. Analysis of these contrasted situations emphasizes the need for future research on the diversity and robustness of plant signaling mechanisms under climate change conditions.

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Quality Control of Photosystem II: The Mechanisms for Avoidance and Tolerance of Light and Heat Stresses are Closely Linked to Membrane Fluidity of the Thylakoids

Cited by 117 publications

References 113 publications

Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus

Thermoacclimation and genome adaptation of the membrane lipidome in marine Synechococcus

Identification of core subunits of photosystem II as action sites of HSP21, which is activated by the GUN5‐mediated retrograde pathway in Arabidopsis

Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

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