An <i>Arabidopsis</i> Mutant with High Cyclic Electron Flow around Photosystem I (<i>hcef</i>) Involving the NADPH Dehydrogenase Complex

Livingston, Aaron K.; Cruz, Jeffrey A.; Kohzuma, Kaori; Dhingra, Amit; Kramer, David

doi:10.1105/tpc.109.071084

Cited by 188 publications

(215 citation statements)

References 79 publications

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“…1, Inset A). These results indicate that the loss of FBPase in hcef1 led to increased H 2 O 2 accumulation, probably resulting from a buildup of reducing intermediates of photosynthetic electron transfer (37), and are consistent with a functional connection between H 2 O 2 and CEF activation.…”

Section: Significancesupporting

confidence: 63%

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

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

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124

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Cyclic electron flow (CEF) around photosystem I is thought to balance the ATP/NADPH energy budget of photosynthesis, requiring that its rate be finely regulated. The mechanisms of this regulation are not well understood. We observed that mutants that exhibited constitutively high rates of CEF also showed elevated production of H 2 O 2 . We thus tested the hypothesis that CEF can be activated by H 2 O 2 in vivo. CEF was strongly increased by H 2 O 2 both by infiltration or in situ production by chloroplastlocalized glycolate oxidase, implying that H 2 O 2 can activate CEF either directly by redox modulation of key enzymes, or indirectly by affecting other photosynthetic processes. CEF appeared with a half time of about 20 min after exposure to H 2 O 2 , suggesting activation of previously expressed CEF-related machinery. H 2 O 2 -dependent CEF was not sensitive to antimycin A or loss of PGR5, indicating that increased CEF probably does not involve the PGR5-PGRL1 associated pathway. In contrast, the rise in CEF was not observed in a mutant deficient in the chloroplast NADPH:PQ reductase (NDH), supporting the involvement of this complex in CEF activated by H 2 O 2 . We propose that H 2 O 2 is a missing link between environmental stress, metabolism, and redox regulation of CEF in higher plants. I n oxygenic photosynthesis, linear electron flow (LEF) is the process by which light energy is captured to drive the extraction of electrons and protons from water and transfer them through a system of electron carriers to reduce NADPH. LEF is coupled to proton translocation into the thylakoid lumen, generating an electrochemical gradient of protons ðΔμ H +Þ or proton motive force (pmf). The pmf drives the synthesis of ATP to power the reactions of the Calvin-Benson-Bassham (CBB) cycle and other essential metabolic processes in the chloroplast. The pmf is also a key regulator of photosynthesis in that it activates the photoprotective q E response to dissipate excess light energy and downregulates electron transfer by controlling the rate of oxidation of plastoquinol at the cytochrome b 6 f complex (b 6 f), thus preventing the buildup of reduced intermediates (1, 2).LEF results in the transfer or deposition into the lumen of three protons for each electron transferred through PSII, plastoquinone (PQ), b 6 f, plastocyanin, and photosystem I (PSI) to ferredoxin (Fd). The synthesis of one ATP is thought to require the passage of 4.67 protons through the ATP synthase, so that LEF should produce a ratio of ATP/NADPH of about 1.33; this ratio is too low to sustain the CBB cycle or supply ATP required for translation, protein transport, or other ATP-dependent processes (3). In addition, the relative demands for ATP and NADPH can change dramatically depending on environmental, developmental, and other factors, leading to rapid energy imbalances that require dynamical regulation of ATP/NADPH balance.Several alternative electron flow pathways in the chloroplast have been proposed to augment ATP production, thus balancing the ATP/NADPH ...

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Section: Significancesupporting

confidence: 63%

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

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

Self Cite

124

116

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“…turnover has led to a proposed role in PSI-dependent cyclic photophosphorylation (Shikanai et al, 1998, Munekage et al, 2004, Livingston et al, 2010, Ifuku et al, 2011. Numerous phenotypic characterizations in Arabidopsis and tobacco have established that under mild conditions of growth, NDH is dispensable , Shikanai et al, 1998, Horváth et al, 2000, Rumeau et al, 2005.…”

Section: Discussionmentioning

confidence: 99%

Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO₂ in the Bundle Sheath Cell of Zea mays

et al. 2016

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Prior studies with Nicotiana and Arabidopsis described failed assembly of the chloroplastic NDH [NAD(P)H dehydrogenase] supercomplex by serial mutation of several subunit genes. We examined the properties of Zea mays leaves containing Mu and Ds insertions into nuclear gene exons encoding the critical O-and N-subunits of NDH, respectively. In vivo reduction of plastoquinone in the dark was sharply diminished in maize homozygous mutant compared to normal leaves but not to the extreme degree observed for the corresponding lesions in Arabidopsis. The net carbon assimilation rate (A) at high irradiance and saturating CO 2 levels was reduced by one-half due to NDH mutation in maize although no genotypic effect was evident at very low CO 2 levels. Simultaneous assessment of chlorophyll fluorescence and A in maize at low (2% by volume) and high (

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“…Maximal PSII quantum efficiency, LEF, and energy-dependent exciton quenching (q E ) were estimated from saturationpulse chlorophyll a fluorescence yield measurements using the instrumentation and methods described previously (33). The value of steady-state fluorescence yield with all PSII centers closed, F M ', was obtained after at least 15 min illumination, at which point the photosynthetic rates and fluorescence parameters were stable.…”

Section: Methodsmentioning

confidence: 99%

Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions

Kohzuma

Bosco

Kanazawa

et al. 2012

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

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The chloroplast ATP synthase catalyzes the light-driven synthesis of ATP and acts as a key feedback regulatory component of photosynthesis. Arabidopsis possesses two homologues of the regulatory γ subunit of the ATP synthase, encoded by the ATPC1 and ATPC2 genes. Using a series of mutants, we show that both these subunits can support photosynthetic ATP synthesis in vivo with similar specific activities, but that in wild-type plants, only γ 1 is involved in ATP synthesis in photosynthesis. The γ 1 -containing ATP synthase shows classical light-induced redox regulation, whereas the mutant expressing only γ 2 -ATP synthase (gamma exchangerevised ATP synthase, gamera) shows equally high ATP synthase activity in the light and dark. In situ redox titrations demonstrate that the regulatory thiol groups on γ 2 -ATP synthase remain reduced under physiological conditions but can be oxidized by the strong oxidant diamide, implying that the redox potential for the thiol/ disulphide transition in γ 2 is substantially higher than that for γ 1 . This regulatory difference may be attributed to alterations in the residues near the redox-active thiols. We propose that γ 2 -ATP synthase functions to catalyze ATP hydrolysis-driven proton translocation in nonphotosynthetic plastids, maintaining a sufficient transthylakoid proton gradient to drive protein translocation or other processes. Consistent with this interpretation, ATPC2 is predominantly expressed in the root, whereas modifying its expression results in alteration of root hair development. Phylogenetic analysis suggests that γ 2 originated from ancient gene duplication, resulting in divergent evolution of functionally distinct ATP synthase complexes in dicots and mosses. plant development | bioenergetics L ight-driven linear electron flow (LEF) in photosynthesis stores energy in reduced NADPH. It is also coupled to the translocation of protons into the thylakoid lumen, generating an electrochemical gradient of protons, the proton motive force (pmf), across the thylakoid. The pmf in turn drives the synthesis of ATP from ATP and P i via the CF O -CF 1 ATP synthase (ATP synthase), storing energy in the form of the photophosphorylation potential. The plastid ATP synthase complex consists of nine different sub-

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An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I (hcef) Involving the NADPH Dehydrogenase Complex

Cited by 188 publications

References 79 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO₂ in the Bundle Sheath Cell of Zea mays

Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions

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An Arabidopsis Mutant with High Cyclic Electron Flow around Photosystem I (hcef) Involving the NADPH Dehydrogenase Complex

Cited by 188 publications

References 79 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO2 in the Bundle Sheath Cell of Zea mays

Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions

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Evidence for a Role for NAD(P)H Dehydrogenase in Concentration of CO₂ in the Bundle Sheath Cell of Zea mays