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Regulation of cyclic and linear electron flow in higher plants.

ABSTRACT: Cyclic electron flow is increasingly recognized as being essential in plant growth, generating a pH gradient across thylakoid membrane (?pH) that contributes to ATP synthesis and triggers the protective process of nonphotochemical quenching (NPQ) under stress conditions. Here, we report experiments demonstrating the importance of that ?pH in protecting plants from stress and relating to the regulation of cyclic relative to linear flow. In leaves infiltrated with low concentrations of nigericin, which dissipates the ?pH without significantly affecting the potential gradient, thereby maintaining ATP synthesis, the extent of NPQ was markedly lower, reflecting the lower ?pH. At the same time, the photosystem (PS) I primary donor P700 was largely reduced in the light, in contrast to control conditions where increasing light progressively oxidized P700, due to down-regulation of the cytochrome bf complex. Illumination of nigericin-infiltrated leaves resulted in photoinhibition of PSII but also, more markedly, of PSI. Plants lacking ferredoxin (Fd) NADP oxidoreductase (FNR) or the polypeptide proton gradient regulation 5 (PGR5) also show reduction of P700 in the light and increased sensitivity to PSI photoinhibition, demonstrating that the regulation of the cytochrome bf complex (cyt bf) is essential for protection of PSI from light stress. The formation of a ?pH is concluded to be essential to that regulation, with cyclic electron flow playing a vital, previously poorly appreciated role in this protective process. Examination of cyclic electron flow in plants with a reduced content of FNR shows that these antisense plants are less able to maintain a steady rate of this pathway. This reduction is suggested to reflect a change in the distribution of FNR from cyclic to linear flow, likely reflecting the formation or disassembly of FNR-cytochrome bf complex.

SUBMITTER: Joliot P

PROVIDER: S-EPMC3156182 | biostudies-literature | 2011 Aug

REPOSITORIES: biostudies-literature

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Regulation of cyclic and linear electron flow in higher plants.

Joliot Pierre P Johnson Giles N GN

Proceedings of the National Academy of Sciences of the United States of America 20110722 32

Cyclic electron flow is increasingly recognized as being essential in plant growth, generating a pH gradient across thylakoid membrane (ΔpH) that contributes to ATP synthesis and triggers the protective process of nonphotochemical quenching (NPQ) under stress conditions. Here, we report experiments demonstrating the importance of that ΔpH in protecting plants from stress and relating to the regulation of cyclic relative to linear flow. In leaves infiltrated with low concentrations of nigericin, ...[more]

PMID: 21784980

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Project description:The Antarctic green alga Chlamydomonas sp. UWO241 (UWO241) survives in the deep photoc zone of the permanently ice-covered Lake Bonney in the McMurdo Dry Valleys. The extreme habitat in its natural environment has given way to unique adaptive mechanisms in this halotolerant psychrophile. One of the most striking phenotype of UWO241 is the constitutive upregulation of cyclic electron flow (CEF) around Photosystem I (PSI). This CEF is associated with the formation of a PSI-cytochrome b6f supercomplex that is stable under conditions of high salinity, corresponding to its natural habitat. Although studies have been done to understand the changes in the photosynthetic apparatus associated with increased CEF, not much is known about the purpose of constitutive CEF in UWO241. In this study, we examined the changes in the metabolism associated with increased in CEF and PSI-supercomplex formation in UWO241 under high salinity. Using Electrochomic Shift (ECS) based spectroscopy we identified a higher NPQ and proton motif flux through ATP synthase associated with UWO241 under high salinity. This higher proton flux was associated with high alternative electron transport when plotted against linear electron flow. We also identified several proteins associated with PSI-cytb6f supercomplex in UWO241 that have not been shown before. A Bestrophin-like protein was identified in the whole cell proteome of UWO241 suggesting high capacity for NPQ. Using comparative shotgun proteomics we identified a total of 98 proteins that were significantly affected under high CEF phenotype in UWO241. Out of the 98 proteins, 46 were upregulated and belonged to Calvin cycle, secondary metabolism and translational machinery. Several enzymes in the secondary metabolic Shikimate pathway were upregulated under high CEF phenotype, with one protein involved in downstream indole acetic acid (IAA) biosynthesis upregulated. Metabolomics revealed upregulation of compatible solutes and downregulation of tryptophan in UWO241 under high salinity. We suggest that UWO241 maintains constitutively high CEF with associated PSI-cytb6f supercomplex under native high salinity conditions to rewire its downstream metabolism towards higher carbon fixation capacity and that fixed carbon is utilized to make secondary metabolites necessary for adaptation in its extreme habitat.

Dataset Information

Regulation of cyclic and linear electron flow in higher plants.

Publications

Regulation of cyclic and linear electron flow in higher plants.

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