The Activity of the Chloroplastic Ndh Complex Is Regulated by Phosphorylation of the NDH-F Subunit

Lascano, Ramiro; Casano, Leonardo M.; Martı́n, Mercedes; Sabater, Bartolomé

doi:10.1104/pp.103.020321

Cited by 67 publications

(69 citation statements)

References 45 publications

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“…3), to involve de novo protein synthesis, which is expected to be considerably slower (60,61), suggesting that short-term H 2 O 2 production can activate preexisting CEF machinery, consistent with a mechanism for rapid activation of CEF to meet fluctuating ATP demands, as proposed earlier (27). In addition, H 2 O 2 was shown in previous studies (29) as well as in this work (Fig.…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 67%

“…These results imply that H 2 O 2 -induced CEF does not involve the PGR5/PGRL1 pathway (4, 6, 7) but favors the involvement of the chloroplast NDH complex, as previously shown in hcef1 (37). Consistent with this view, accumulation and phosphorylation of the NDH complex has been associated with increased activity in the presence of oxidative stress (27,29), and its activation results in increased postillumination fluorescence rise, which was increased in the GO5 mutant (Fig. S6). A Regulatory Role for H 2 O 2 in Activation of CEF?…”

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 67%

“…Based on in vitro studies, it was previously proposed that H 2 O 2 could activate CEF or chlororespiration by modifying the NDH complex (27). It has also been shown that H 2 O 2 can increase the expression of the NDH complex (29) and may further affect the accumulation of photosynthetic metabolites, indirectly activating CEF (26).…”

Section: Significancementioning

confidence: 99%

“…Other possible regulatory mechanisms include sensing of ATP/ADP ratios (23,24), the redox status of NAD(P)H or Fd (25), various CBB metabolic intermediates (reviewed in ref. 26), calcium signaling (15,27), phosphorylation of CEF-related proteins (27), and the reactive oxygen species H 2 O 2 (26)(27)(28)(29).…”

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confidence: 99%

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Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

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

119

116

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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: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 67%

Section: Effects Of H 2 O 2 Production By Plants Expressing Glycolatesupporting

confidence: 67%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Activation of cyclic electron flow by hydrogen peroxide in vivo

Strand

Livingston

Satoh-Cruz

et al. 2015

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

119

116

View full text Add to dashboard Cite

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“…15,21,[23][24][25] These increases are accompanied by an increase of thylakoid peroxidase but not of SOD, 12,23 in contrast to the response of young leaves in which the three chlororespiratory activities increase in response to different stress situations. By increasing the level of the reduced forms of electron transporters, the increase of Ndh in senescent leaves must increase the rate of the Mehler reaction producing Á O 2 À .…”

Section: Introductionmentioning

confidence: 84%

Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco

et al. 2005

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Mitochondrial involvement has not been identified in the programmed cell death (PCD) of leaf senescence which suggests that processes such as those involving reactive oxygen species (ROS) are controlled by chloroplasts. We report that transgenic tobacco (DndhF), with the plastid ndhF gene knocked-out, shows low levels of the plastid Ndh complex, homologous to mitochondrial complex I, and more than a 30-day-delay in leaf senescence with respect to wt. The comparison of activities and protein levels and analyses of genetic and phenotypic traits of wtxDndhF crosses indicate that regulatory roles of mitochondria in animal PCD are assumed by chloroplasts in leaf senescence. The Ndh complex would increase the reduction level of electron transporters and the generation of ROS. Chloroplastic control of leaf senescence provides a nonclassical model of PCD and reveals an unexpected role of the plastid ndh genes that are present in most higher plants.

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Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

Strand

Kramer

et al. 2018

Plant Direct

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Sigma factor (SIG) proteins contribute to promoter specificity of the plastid‐encoded RNA polymerase during chloroplast genome transcription. All six members of the SIG family, that is, SIG1–SIG6, are nuclear‐encoded proteins targeted to chloroplasts. Sigma factor 2 (SIG2) is a phytochrome‐regulated protein important for stoichiometric control of the expression of plastid‐ and nuclear‐encoded genes that impact plastid development and plant growth and development. Among SIG factors, SIG2 is required not only for transcription of chloroplast genes (i.e., anterograde signaling), but also impacts nuclear‐encoded, photosynthesis‐related, and light signaling‐related genes (i.e., retrograde signaling) in response to plastid functional status. Although SIG2 is involved in photomorphogenesis in Arabidopsis, the molecular bases for its role in light signaling that impacts photomorphogenesis and aspects of photosynthesis have only recently begun to be investigated. Previously, we reported that SIG2 is necessary for phytochrome‐mediated photomorphogenesis specifically under red (R) and far‐red light, thereby suggesting a link between phytochromes and nuclear‐encoded SIG2 in light signaling. To explore transcriptional roles of SIG2 in R‐dependent growth and development, we performed RNA sequencing analysis to compare gene expression in sig2‐2 mutant and Col‐0 wild‐type seedlings at two developmental stages (1‐ and 7‐day). We identified a subset of misregulated genes involved in growth, hormonal cross talk, stress responses, and photosynthesis. To investigate the functional relevance of these gene expression analyses, we performed several comparative phenotyping tests. In these analyses, strong sig2 mutants showed insensitivity to bioactive GA3, high intracellular levels of hydrogen peroxide (H2O2) indicative of a stress response, and specific defects in photosynthesis, including elevated levels of cyclic electron flow (CEF) and nonphotochemical quenching (NPQ). We demonstrated that SIG2 regulates a broader range of physiological responses at the molecular level than previously reported, with specific roles in red‐light‐mediated photomorphogenesis.

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The Activity of the Chloroplastic Ndh Complex Is Regulated by Phosphorylation of the NDH-F Subunit

Cited by 67 publications

References 45 publications

Activation of cyclic electron flow by hydrogen peroxide in vivo

Activation of cyclic electron flow by hydrogen peroxide in vivo

Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco

Transcriptome and phenotyping analyses support a role for chloroplast sigma factor 2 in red‐light‐dependent regulation of growth, stress, and photosynthesis

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