Quality control of Photosystem II: Where and how does the degradation of the D1 protein by FtsH proteases start under light stress? – Facts and hypotheses

Yoshioka, Miho; Yamamoto, Yasutake

doi:10.1016/j.jphotobiol.2011.01.016

Cited by 33 publications

(32 citation statements)

References 41 publications

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“…In this study, those four proteases were identified in both thylakoid subcompartments, with a strong enrichment in the stroma-lamellae. This is in good agreement with recent data showing that Ftsh proteins were present in both thylakoid subcompartments, as monomers and homo/heteromeric dimers in stromal region and as hexameric complexes in the grana regions (94). The thylakoid located Ftsh complex in Arabidopsis is responsible for degradation of photodamaged D1 protein (PsbA) in concert with lumenal Deg proteases (see for reviews (95,96)).…”

Section: Discussionsupporting

confidence: 91%

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Tomizioli

Lazar

Brugière

et al. 2014

Molecular & Cellular Proteomics

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Photosynthesis has shaped atmospheric and ocean chemistries and probably changed the climate as well, as oxygen is released from water as part of the photosynthetic process. In photosynthetic eukaryotes, this process occurs in the chloroplast, an organelle containing the most abundant biological membrane, the thylakoids. The thylakoids of plants and some green algae are structurally inhomogeneous, consisting of two main domains: the grana, which are piles of membranes gathered by stacking forces, and the stroma-lamellae, which are unstacked thylakoids connecting the grana. The major photosynthetic complexes are unevenly distributed within these compartments because of steric and electrostatic constraints. Although proteomic analysis of thylakoids has been instrumental to define its protein components, no extensive proteomic study of subthylakoid localization of proteins in the BBY (grana) and the stroma-lamellae fractions has been achieved so far. To fill this gap, we performed a complete survey of the protein composition of these thylakoid subcompartments using thylakoid membrane fractionations. We employed semiquantitative proteomics coupled with a data analysis pipeline and manual annotation to differentiate genuine BBY and stroma-lamellae proteins from possible contaminants. About 300 thylakoid (or potentially thylakoid) proteins were shown to be enriched in either the BBY or the stroma-lamellae fractions. Overall, present findings corroborate previous observations obtained for photosynthetic proteins that used nonproteomic approaches. The originality of the present proteomic relies in the identification of photosynthetic proteins whose differential distribution in the thylakoid subcompartments might explain already observed phenomenon such as LHCII docking. Besides, from the present localization results we can suggest new molecular actors for photosynthesis-linked activities. For instance, most PsbP-like subunits being differently localized in stroma-lamellae, these proteins could be linked to the PSI-NDH complex in the context of cyclic electron flow around PSI. In addition, we could identify about a hundred new likely minor thylakoid (or chloroplast) proteins, some of them being potential regulators of the chloroplast physiology. Molecular & Cellular Proteomics 13: 10.1074/mcp.M114.040923, 2147-2167, 2014.As primary producers, plants are at the basis of the food chain for most ecosystems and control the planet atmosphere via photosynthesis. In eukaryotes, this process, responsible for carbon fixation and for the release of gaseous oxygen into the atmosphere, takes place in a specialized compartment, the chloroplast. This semiautonomous organelle plays a number of essential functions, including photosynthesis, nitrogen assimilation, sulfur reduction and assimilation, synthesis of amino acids, fatty acids, and many secondary metabolites (1-6). The chloroplast is not the only type of plastids. Plastids are indeed found in every plant tissue (with a very few exceptions such as angiosperm pollen grains) and in...

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Section: Discussionsupporting

confidence: 91%

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Tomizioli

Lazar

Brugière

et al. 2014

Molecular & Cellular Proteomics

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“…This large protrusion may exclude the FtsH proteases from stacked regions by steric hindrances, because ultrastructural data showed an only 3-to 4-nm wide partition gap in grana (26,42). Intermixing of FtsH proteases and photoinhibited PSII by partial lateral destacking is favorable for a swift D1 degradation, as postulated recently (43,44).…”

Section: Discussionsupporting

confidence: 66%

Architectural switch in plant photosynthetic membranes induced by light stress

Herbstová

Tietz

Kinzel

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

143

113

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Unavoidable side reactions of photosynthetic energy conversion can damage the water-splitting photosystem II (PSII) holocomplex embedded in the thylakoid membrane system inside chloroplasts. Plant survival is crucially dependent on an efficient molecular repair of damaged PSII realized by a multistep repair cycle. The PSII repair cycle requires a brisk lateral protein traffic between stacked grana thylakoids and unstacked stroma lamellae that is challenged by the tight stacking and low protein mobility in grana. We demonstrated that high light stress induced two main structural changes that work synergistically to improve the accessibility between damaged PSII in grana and its repair machinery in stroma lamellae: lateral shrinkage of grana diameter and increased protein mobility in grana thylakoids. It follows that high light stress triggers an architectural switch of the thylakoid network that is advantageous for swift protein repair. Studies of the thylakoid kinase mutant stn8 and the double mutant stn7/8 demonstrate the central role of protein phosphorylation for the structural alterations. These findings are based on the elaboration of mathematical tools for analyzing confocal laser-scanning microscopic images to study changes in the sophisticated thylakoid architecture in intact protoplasts.confocal microscopy | macromolecular crowding | photosynthesis P hotosynthetic transformation of sunlight into metabolic energy equivalents is a dangerous venture, because toxic side products of the primary photochemical processes can lead to uncontrolled damage. Harmful photosynthetic side reactions cannot be avoided completely and become a serious problem under stress (e.g., high light stress). The main target of photoinhibition (PI) is the D1 subunit of the water-splitting photosystem II (PSII) (1, 2). The D1 subunit is buried in the massive (1,400 kDa) PSII holocomplex that is organized as a dimer and binds between two and four trimeric light-harvesting complex IIs (LHCIIs) (3, 4). Estimates predict that without repair of damaged PSII, the efficiency for photosynthetic energy conversion would drop below 5% (5). Consequently, plants would not survive in a highly dynamic and competitive natural environment. Plants address this challenge through the evolutionary invention of one of the fastest and most efficient molecular repair mechanisms in nature, the PSII repair cycle (5-7).The PSII repair cycle consist of a series of events, including phosphorylation/ dephosphorylation of PSII subunits, holocomplex disassembly/reassembly, and D1 degradation/de novo synthesis (8-10). All of these reactions are harbored in or at the thylakoid membrane system inside the chloroplast. The complex folding of the thylakoid membrane leads to a structural differentiation into stacked grana regions interconnected by unstacked stroma lamellae (11)(12)(13). This structural heterogeneity is accompanied by, and partly driven by, differential protein distributions. PSII and LHCII are concentrated in grana stacks, photosystem I (PSI) and the ATPas...

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“…These results are in contrast to several photoinhibition studies performed with Arabidopsis showing that PSII protein turnover required both the involvement of FtsH and Deg/Htr proteases (Itzhaki et al, 1998;Kapri-Pardes et al, 2007;Sun et al, 2007). High-light treatment was reported to increase the expression of Deg/Htr and FtsH types of proteases in Arabidopsis (Sinvany- Villalobo et al, 2004), to raise the level of FtsH hexamerization and unstacking of thylakoids (reviewed in Yoshioka and Yamamoto, 2011), and to activate the lumenal Deg protease, based on in vitro experiments showing its hexamerization upon acidification (Kley et al, 2011). Thus, a model for D1 degradation in the chloroplast was proposed in which Deg proteases act as endoproteases fragmenting D1 and FtsH proteases act as exoproteases processively degrading D1 and its fragments (reviewed in ).…”

Section: Ftsh1 Regulates the Degradation Of Psii Upon Photoinhibitioncontrasting

confidence: 56%

Thylakoid FtsH Protease Contributes to Photosystem II and Cytochromeb 6 fRemodeling inChlamydomonas reinhardtiiunder Stress Conditions

et al. 2014

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FtsH is the major thylakoid membrane protease found in organisms performing oxygenic photosynthesis. Here, we show that FtsH from Chlamydomonas reinhardtii forms heterooligomers comprising two subunits, FtsH1 and FtsH2. We characterized this protease using FtsH mutants that we identified through a genetic suppressor approach that restored phototrophic growth of mutants originally defective for cytochrome b 6 f accumulation. We thus extended the spectrum of FtsH substrates in the thylakoid membranes beyond photosystem II, showing the susceptibility of cytochrome b 6 f complexes (and proteins involved in the c i heme binding pathway to cytochrome b 6 ) to FtsH. We then show how FtsH is involved in the response of C. reinhardtii to macronutrient stress. Upon phosphorus starvation, photosynthesis inactivation results from an FtsH-sensitive photoinhibition process. In contrast, we identified an FtsH-dependent loss of photosystem II and cytochrome b 6 f complexes in darkness upon sulfur deprivation. The D1 fragmentation pattern observed in the latter condition was similar to that observed in photoinhibitory conditions, which points to a similar degradation pathway in these two widely different environmental conditions. Our experiments thus provide extensive evidence that FtsH plays a major role in the quality control of thylakoid membrane proteins and in the response of C. reinhardtii to light and macronutrient stress.

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Quality control of Photosystem II: Where and how does the degradation of the D1 protein by FtsH proteases start under light stress? – Facts and hypotheses

Cited by 33 publications

References 41 publications

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach

Architectural switch in plant photosynthetic membranes induced by light stress

Thylakoid FtsH Protease Contributes to Photosystem II and Cytochromeb 6 fRemodeling inChlamydomonas reinhardtiiunder Stress Conditions

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