Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

Kirchhoff, Helmut

doi:10.1098/rstb.2013.0225

Cited by 105 publications

(89 citation statements)

References 68 publications

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“…For dark-adapted samples, the FtsH protease concentration is highest in grana margins, about 50% lower in stroma lamellae, and very low in the grana core regions. The very low abundance in grana core membranes is in line with the literature (21,23,29) and can be explained by the bulky stromal protrusion of the FtsH hexamer, which sterically restricts access of the protease to tightly stacked grana regions (30). In HL-treated protoplasts, the abundance of FtsH in grana core is also very low, indicating that the stromal partition gap in grana core does not widen in HL (in agreement with the EM analysis in Fig.…”

supporting

confidence: 89%

Compartmentalization of the protein repair machinery in photosynthetic membranes

Puthiyaveetil

Tsabari

Lowry

et al. 2014

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

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A crucial component of protein homeostasis in cells is the repair of damaged proteins. The repair of oxygen-evolving photosystem II (PS II) supercomplexes in plant chloroplasts is a prime example of a very efficient repair process that evolved in response to the high vulnerability of PS II to photooxidative damage, exacerbated by high-light (HL) stress. Significant progress in recent years has unraveled individual components and steps that constitute the PS II repair machinery, which is embedded in the thylakoid membrane system inside chloroplasts. However, an open question is how a certain order of these repair steps is established and how unwanted back-reactions that jeopardize the repair efficiency are avoided. Here, we report that spatial separation of key enzymes involved in PS II repair is realized by subcompartmentalization of the thylakoid membrane, accomplished by the formation of stacked grana membranes. The spatial segregation of kinases, phosphatases, proteases, and ribosomes ensures a certain order of events with minimal mutual interference. The margins of the grana turn out to be the site of protein degradation, well separated from active PS II in grana core and de novo protein synthesis in unstacked stroma lamellae. Furthermore, HL induces a partial conversion of stacked grana core to grana margin, which leads to a controlled access of proteases to PS II. Our study suggests that the origin of grana in evolution ensures high repair efficiency, which is essential for PS II homeostasis.photosynthesis | photoinhibition | PS II repair cycle | thylakoid membrane | grana margin R epair of damaged protein complexes is essential for the survival of all living organisms. One of nature's most efficient repair machineries is localized in photosynthetic thylakoid membranes of plants, which can turn over the total pool of the watersplitting photosystem II (PS II) supercomplex in less than 1 h (1). This remarkable potential for protein repair is crucial for the survival and fitness of plants because photodamage by reactive oxygen species is an inherent feature of PS II photochemistry. Significant knowledge gained over the past decade identifies individual steps involved in PS II repair. This progress has led to the formulation of a repair cycle that describes the life cycle of PS II, proceeding from its damage, disassembly, degradation, and resynthesis to its reassembly (2-4).To appreciate the challenges for repairing damaged PS II, it is essential to understand two structural features of the thylakoid membrane system. The first is that functional PS II is organized as a dimeric 1.4-MDa supercomplex in which each monomer consists of at least 28 subunits with two trimeric light harvesting complexes II (LHC II) attached to the core (5, 6). Within this huge supercomplex, the main target of photodamage is the central D1 subunit (7). The PS II repair cycle is therefore mainly designed for specific replacement of the damaged D1, which requires disassembly and reassembly of the whole supercomplex. The second characteri...

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supporting

confidence: 89%

Compartmentalization of the protein repair machinery in photosynthetic membranes

Puthiyaveetil

Tsabari

Lowry

et al. 2014

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

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“…It is possible that our conditions led to a more complete antenna dephosphorylation in state 1. The availability of the Lhcbs as substrates for the kinase may change under different light conditions (Zer et al, 2003;Kirchhoff, 2014). Furthermore, Lhcb2 is less abundant than Lhcb1.…”

Section: Discussion Phosphorylation Kinetics Of Lhcb1 and Lhcb2mentioning

confidence: 99%

“…Indeed, after BN-PAGE, a large proportion of LHCII is in the form of free trimers, which are most likely loosely bound in supercomplexes in vivo (Caffarri et al, 2009;Järvi et al, 2011;Pagliano et al, 2014;Grieco et al, 2015). Furthermore, PSII supercomplexes in the grana core may not be accessible to phosphorylation for steric reasons, because the tight appression of the membranes could hinder the access of the corresponding protein kinases (Zer et al, 2003;Kirchhoff, 2014).…”

Section: Antenna Phosphorylation In the Psi-lhcii State Transition Sumentioning

confidence: 99%

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

et al. 2015

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ORCID IDs: 0000-0003-0587-7621 (P.L.); 0000-0002-6155-9153 (D.D.).Light-harvesting complex II (LHCII) is a crucial component of the photosynthetic machinery, with central roles in light capture and acclimation to changing light. The association of an LHCII trimer with PSI in the PSI-LHCII supercomplex is strictly dependent on LHCII phosphorylation mediated by the kinase STATE TRANSITION7, and is directly related to the light acclimation process called state transitions. In Arabidopsis (Arabidopsis thaliana), the LHCII trimers contain isoforms that belong to three classes: Lhcb1, Lhcb2, and Lhcb3. Only Lhcb1 and Lhcb2 can be phosphorylated in the N-terminal region. Here, we present an improved Phos-tag-based method to determine the absolute extent of phosphorylation of Lhcb1 and Lhcb2. Both classes show very similar phosphorylation kinetics during state transition. Nevertheless, only Lhcb2 is extensively phosphorylated (.98%) in PSI-LHCII, whereas phosphorylated Lhcb1 is largely excluded from this supercomplex. Both isoforms are phosphorylated to different extents in other photosystem supercomplexes and in different domains of the thylakoid membranes. The data imply that, despite their high sequence similarity, differential phosphorylation of Lhcb1 and Lhcb2 plays contrasting roles in light acclimation of photosynthesis.

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“…It is generally agreed that NPQ requires the structural flexibility of thylakoid membranes. In fact, there are several reports demonstrating the involvement of structural changes at different levels of structural complexity [4][5][6][7][8][9][10][11][12][13][14]. Some of these changes might be directly linked to the generation of ∆pH, e.g., via the redistribution of ions in the 'electrolyte' following the generation of ∆µ H + [15,16] and, in particular, upon the acidification of lumen and the binding of protons to different polypeptide residues [2,17,18].…”

Section: Introductionmentioning

confidence: 99%

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

Ünnep¹,

Zsíros²,

Hörcsik³

et al. 2017

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Energization of thylakoid membranes brings about the acidification of the lumenal aqueous phase, which activates important regulatory mechanisms. Earlier Jajoo and coworkers (2014 FEBS Lett. 588:970) have shown that low pH in isolated plant thylakoid membranes induces changes in the excitation energy distribution between the two photosystems. In order to elucidate the structural background of these changes, we used small-angle neutron scattering on thylakoid membranes exposed to low p 2 H (pD) and show that gradually lowering the p 2 H from 8.0 to 5.0 causes small but well discernible reversible diminishment of the periodic order and the lamellar repeat distance and an increased mosaicity -similar to the effects elicited by light-induced acidification of the lumen. Our data strongly suggest that thylakoids dynamically respond to the membrane energization and actively participate in different regulatory mechanisms. Keywords: chloroplast thylakoid membranes, lamellar repeat distance, low pH and p 2 H, smallangle neutron scattering (SANS) Highlights:1. Thylakoid membranes exposed to low p 2 H studied by small-angle neutron scattering 2. Acidification causes reversible shrinkage and diminished lamellar order 3. SANS changes induced by low pH resemble those due to light-induced lumenal acidification Abbreviations: p 2 H (pD), deuterium analogue of pH; NPQ, non-photochemical quenching; qE, the energy-dependent component of NPQ; ∆µ H + , transmembrane electrochemical potential gradient; PSI, photosystem I; PSII, photosystem II; LET, linear electron transport; CD, circular dichroism; SANS, small-angle neutron scattering; q, scattering vector; I, intensity; q*, center position of the Bragg peak; RD, repeat distance; φ, azimuthal angle; I(φ), angular dependency of the scattering intensity; FWHM, full width at half maximum 3

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Structural changes of the thylakoid membrane network induced by high light stress in plant chloroplasts

Cited by 105 publications

References 68 publications

Compartmentalization of the protein repair machinery in photosynthetic membranes

Compartmentalization of the protein repair machinery in photosynthetic membranes

Phosphorylation of the Lhcb2 isoform of Light Harvesting Complex II is central to state transitions

Low-pH induced reversible reorganizations of chloroplast thylakoid membranes — As revealed by small-angle neutron scattering

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