Temperature-dependent regulation of electron transport and ATP synthesis in chloroplasts in vitro and in silico

Тихонов, А. Н.; Vershubskii, A. V.

doi:10.1007/s11120-020-00777-0

Cited by 14 publications

(7 citation statements)

References 167 publications

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“…In particular, all data suggest that the elevation of temperature, from 5 to 15 or 25 °C, largely destabilizes the bilayers and increases the contributions of the non-bilayer lipid phases, parallel with substantial rises in the permeability of the membrane, due to basal ion fluxes [ 6 ]. As inferred from the literature data [ 83 , 84 ] and own unpublished measurements, in the physiological temperature interval, parallel with the enhancements of the non-bilayer lipid phases (and increased membrane permeability and fluidity), the rates of electron transport and synthesis of ATP increase. It is unclear if these apparently opposite effects arise merely from a ‘compromise’ between the energy transduction and the structural flexibility of membranes.…”

Section: Discussionmentioning

confidence: 60%

Lipid Polymorphism of the Subchloroplast—Granum and Stroma Thylakoid Membrane–Particles. II. Structure and Functions

Dlouhý

Karlický

Arshad

et al. 2021

Cells

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In Part I, by using 31P-NMR spectroscopy, we have shown that isolated granum and stroma thylakoid membranes (TMs), in addition to the bilayer, display two isotropic phases and an inverted hexagonal (HII) phase; saturation transfer experiments and selective effects of lipase and thermal treatments have shown that these phases arise from distinct, yet interconnectable structural entities. To obtain information on the functional roles and origin of the different lipid phases, here we performed spectroscopic measurements and inspected the ultrastructure of these TM fragments. Circular dichroism, 77 K fluorescence emission spectroscopy, and variable chlorophyll-a fluorescence measurements revealed only minor lipase- or thermally induced changes in the photosynthetic machinery. Electrochromic absorbance transients showed that the TM fragments were re-sealed, and the vesicles largely retained their impermeabilities after lipase treatments—in line with the low susceptibility of the bilayer against the same treatment, as reflected by our 31P-NMR spectroscopy. Signatures of HII-phase could not be discerned with small-angle X-ray scattering—but traces of HII structures, without long-range order, were found by freeze-fracture electron microscopy (FF-EM) and cryo-electron tomography (CET). EM and CET images also revealed the presence of small vesicles and fusion of membrane particles, which might account for one of the isotropic phases. Interaction of VDE (violaxanthin de-epoxidase, detected by Western blot technique in both membrane fragments) with TM lipids might account for the other isotropic phase. In general, non-bilayer lipids are proposed to play role in the self-assembly of the highly organized yet dynamic TM network in chloroplasts.

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Section: Discussionmentioning

confidence: 60%

Lipid Polymorphism of the Subchloroplast—Granum and Stroma Thylakoid Membrane–Particles. II. Structure and Functions

Dlouhý

Karlický

Arshad

et al. 2021

Cells

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“…Of particular interest is their possible role in membrane energization and the utilization of the proton motive force. It is an intriguing fact that the relative contributions of non-bilayer lipid phases significantly increase with the elevation in the temperature in the physiological range [ 18 , 31 ], parallel with the increase in the photosynthetic electron transport rate [ 93 , 94 ]. It is interesting to point out that in mitochondrial membranes, the temperature-dependent synthesis of ATP shows a positive correlation with the emergence of a non-bilayer lipid phase [ 20 ].…”

Section: Discussionmentioning

confidence: 99%

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Dlouhý

Karlický

Javornik

et al. 2022

Cells

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It is well established that plant thylakoid membranes (TMs), in addition to a bilayer, contain two isotropic lipid phases and an inverted hexagonal (HII) phase. To elucidate the origin of non-bilayer lipid phases, we recorded the 31P-NMR spectra of isolated spinach plastoglobuli and TMs and tested their susceptibilities to lipases and proteases; the structural and functional characteristics of TMs were monitored using biophysical techniques and CN-PAGE. Phospholipase-A1 gradually destroyed all 31P-NMR-detectable lipid phases of isolated TMs, but the weak signal of isolated plastoglobuli was not affected. Parallel with the destabilization of their lamellar phase, TMs lost their impermeability; other effects, mainly on Photosystem-II, lagged behind the destruction of the original phases. Wheat-germ lipase selectively eliminated the isotropic phases but exerted little or no effect on the structural and functional parameters of TMs—indicating that the isotropic phases are located outside the protein-rich regions and might be involved in membrane fusion. Trypsin and Proteinase K selectively suppressed the HII phase—suggesting that a large fraction of TM lipids encapsulate stroma-side proteins or polypeptides. We conclude that—in line with the Dynamic Exchange Model—the non-bilayer lipid phases of TMs are found in subdomains separated from but interconnected with the bilayer accommodating the main components of the photosynthetic machinery.

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“…High temperatures can trigger photosystem damage (Yamamoto et al, 2008), chlorophyll degradation, and reduced rates of ribulose 1,5‐bisphosphate carboxylase/oxygenase regeneration (Salvucci & Crafts‐Brandner, 2004), all of which impede the photosynthetic efficiency. Heat stress makes it more difficult for plants to maintain a proton motive force (pmf) across the thylakoid membrane owing to interrupted electron transport, increased ATP synthase activity at high temperatures, and proton leakage from the thylakoid lumen due to membrane fluidization (Tikhonov & Vershubskii, 2020). The pmf has two components: transmembrane potential (Δψ) and proton gradient (ΔpH).…”

Section: Introductionmentioning

confidence: 99%

Chloroplast inner envelope protein FtsH11 is involved in the adjustment of assembly of chloroplast ATP synthase under heat stress

Yue

Shi

et al. 2023

Plant Cell & Environment

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The maintenance of a proton gradient across the thylakoid membrane is an integral aspect of photosynthesis that is mainly established by the splitting of water molecules in photosystem II and plastoquinol oxidation at the cytochrome complex, and it is necessary for the generation of ATP in the last step of photophosphorylation. Although environmental stresses, such as high temperatures, are known to disrupt this fundamental process, only a few studies have explored the molecular mechanisms underlying proton gradient regulation during stress. The present study identified a heat‐sensitive mutant that displays aberrant photosynthesis at high temperatures. This mutation was mapped to AtFtsH11, which encodes an ATP‐dependent AAA‐family metalloprotease. We showed that AtFtsH11 localizes to the chloroplast inner envelope membrane and is capable of degrading the ATP synthase assembly factor BFA3 under heat stress. We posit that this function limits the amount of ATP synthase integrated into the thylakoid membrane to regulate proton efflux from the lumen to the stroma. Our data also suggest that AtFtsH11 is critical in stabilizing photosystem II and cytochrome complexes at high temperatures, and additional studies can further elucidate the specific molecular functions of this critical regulator of photosynthetic thermotolerance.

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Temperature-dependent regulation of electron transport and ATP synthesis in chloroplasts in vitro and in silico

Cited by 14 publications

References 167 publications

Lipid Polymorphism of the Subchloroplast—Granum and Stroma Thylakoid Membrane–Particles. II. Structure and Functions

Lipid Polymorphism of the Subchloroplast—Granum and Stroma Thylakoid Membrane–Particles. II. Structure and Functions

Structural Entities Associated with Different Lipid Phases of Plant Thylakoid Membranes—Selective Susceptibilities to Different Lipases and Proteases

Chloroplast inner envelope protein FtsH11 is involved in the adjustment of assembly of chloroplast ATP synthase under heat stress

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