Depletion of stromal Pi induces high ‘energy‐dependent’ antenna exciton quenching (qE) by decreasing proton conductivity at CFO‐CF1 ATP synthase

Takizawa, Kayoko; Kanazawa, Atsuko; Kramer, David

doi:10.1111/j.1365-3040.2007.01753.x

Cited by 128 publications

(114 citation statements)

References 47 publications

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“…There is also evidence that decreased ATP synthesis itself results in decreased ATP levels, slowing RuBP regeneration, which in turn limits Rubisco and PSII activity. These results are consistent with regulation via stromal P i , as previously proposed Sharkey 1990;Kanazawa and Kramer 2002;Takizawa et al 2008), or alternatively by an allosteric regulator of ATP synthase, which responds similarly. In this way, the ATP synthase may act as a central co-regulator of the light and dark reactions of photosynthesis.…”

Section: Discussionsupporting

confidence: 80%

“…The linear relationships seen in Figs 4b, c and 7b show that the likely path of feedback control is as predicted earlier Sharkey 1990;Takizawa et al 2008): metabolic events lead to the slowing of the ATP synthase, leading to acidification of the lumen pH and subsequent slowing of LEF at the cyt b 6 f complex. The same lumen acidification also activates the q E response (Fig.…”

Section: Downregulation Of the Atp Synthase Under Feedbacklimiting Comentioning

confidence: 63%

“…Under certain conditions, the light reactions of photosynthesis are regulated by modulating the activity of the ATP synthase, possible by altering the concentration of P i in the stroma (reviewed in Takizawa et al 2008). It is generally accepted that the concentration of P i in the chloroplast stroma is an important regulator of processes in photosynthesis Sharkey 1990).…”

Section: Introductionmentioning

confidence: 99%

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Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase

Kiirats

Cruz

Edwards

et al. 2009

Functional Plant Biol.

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Abstract.It was previously shown that photosynthetic electron transfer is controlled under low CO 2 via regulation of the chloroplast ATP synthase. In the current work, we studied the regulation of photosynthesis under feedback limiting conditions, where photosynthesis is limited by the capacity to utilise triose-phosphate for synthesis of end products (starch or sucrose), in a starch-deficient mutant of Nicotiana sylvestris Speg. & Comes. At high CO 2 , we observed feedback control that was progressively reversed by increasing O 2 levels from 2 to 40%. The activity of the ATP synthase, probed in vivo by the dark-interval relaxation kinetics of the electrochromic shift, was proportional to the O 2 -induced increases in O 2 evolution from PSII (J O 2 ), as well as the sum of Rubisco oxygenation (v o ) and carboxylation (v c ) rates. The altered ATP synthase activity led to changes in the light-driven proton motive force, resulting in regulation of the rate of plastoquinol oxidation at the cytochrome b 6 f complex, quantitatively accounting for the observed control of photosynthetic electron transfer. The ATP content of the cell decreases under feedback limitation, suggesting that the ATP synthesis was downregulated to a larger extent than ATP consumption. This likely resulted in slowing of ribulose bisphosphate regeneration and J O 2 ). Overall, our results indicate that, just as at low CO 2 , feedback limitations control the light reactions of photosynthesis via regulation of the ATP synthase, and can be reconciled with regulation via stromal P i , or an unknown allosteric affector.Additional keywords: electrochromic shift, in vivo spectroscopy, non-photochemical, proton motive force, quenching, regulation.

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Section: Discussionsupporting

confidence: 80%

Section: Downregulation Of the Atp Synthase Under Feedbacklimiting Comentioning

confidence: 63%

Section: Introductionmentioning

confidence: 99%

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Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase

Kiirats

Cruz

Edwards

et al. 2009

Functional Plant Biol.

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“…It has been suggested that if such an activity sequesters stromal Pi below the K m of the thylakoid ATP synthase, the resulting decrease in proton conductivity could serve as a means of down regulating photosynthetic light capture. 4,38 The PHT4;1 promoter also exhibited weak activity in the root stele (Fig. 1g), which corroborates previous results indicating that endogenous transcripts are present in roots at low levels.…”

Section: Discussionsupporting

confidence: 79%

Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues

Guo

Irigoyen

Fowler

et al. 2008

Plant Signaling & Behavior

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Plastids rely on multiple phosphate (Pi) transport activities to support and control a wide range of metabolic processes, including photosynthesis and carbon partitioning. Five of the six members of the PHT4 family of Pi transporters in Arabidopsis thaliana (PHT4;1-PHT4;5) are confirmed or predicted plastid proteins. As a step towards identifying the roles of individual PHT4 Pi transporters in chloroplast and non-photosynthetic plastid Pi dynamics, we used promoter-reporter gene fusions and quantitative RT-PCR studies, respectively, to determine spatial and diurnal gene expression patterns. PHT4;1 and PHT4;4 were both expressed predominantly in photosynthetic tissues, although expression of PHT4;1 was circadian and PHT4;4 was induced by light. PHT4;3 and PHT4;5 were expressed mainly in leaf phloem. PHT4;2 was expressed throughout the root, and exhibited a diurnal pattern with peak transcript levels in the dark. The remaining member of this gene family, PHT4;6, encodes a Golgi-localized protein and was expressed ubiquitously. The overlapping but distinct expression patterns for these genes suggest specialized roles for the encoded transporters in multiple types of differentiated plastids. Phylogenetic analysis revealed conservation of each of the orthologous members of the PHT4 family in Arabidopsis and rice, which is consistent with specialization, and suggests that the individual members of this transporter family diverged prior to the divergence of monocots and dicots. IntroductionDynamic control of stromal inorganic phosphate (Pi) levels is central to the specialized metabolic functions of differentiated plastids. Notably, the concentration of Pi in the chloroplast stroma is tightly coordinated with environmental conditions to modulate both photosynthesis and the subsequent partitioning of fixed carbon. 1,2 Pi concentrations in amyloplasts also are held within a critical limit to prevent inhibition of starch biosynthesis. 3 For each plastid type, Pi concentrations are controlled through a combination of metabolic recycling in the stroma and surrounding cytosol, and the transport of Pi across the plastid limiting membrane. Recent data suggest that similar processes also link the Pi status of the chloroplast stroma and thylakoid lumen. 4 Plastidic Pi transport is generally attributed to members of the plastidic phosphate translocator (pPT) family. 5 These proteins are located in the inner envelope membrane and mediate strict counterexchange of Pi for phosphorylated C3, C5 or C6 compounds. The triose phosphate/Pi translocator (TPT) was the first pPT protein to be identified, and it is expressed almost exclusively in photosynthetic tissues where it catalyzes transport of cytosolic Pi into the chloroplast in exchange for triose phosphates, the end products of photosynthesis. 6 This activity represents the major pathway for carbon allocation to the cytosol during the day as well as the primary route for Pi import into the chloroplast. Related members of the pPT family include the phosphoenolpyruvate/Pi translocator...

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“…We found that reductions in ATP synthase content increased NPQ and probably the transthylakoid DpH as previously reported (Price et al, 1995). It has also been suggested that ATP synthase senses the status of stromal metabolites either directly or indirectly (Kramer et al, 2004) and it has been suggested that its activity can be modulated by altering Pi levels (Kanazawa and Kramer, 2002;Takizawa et al, 2008). A number of Calvin cycle enzyme activities are regulated by the chloroplast ferredoxin-thioredoxin pathway (e.g.…”

Section: Atp Synthase Activity Varies In Vivosupporting

confidence: 59%

The Roles of ATP Synthase and the Cytochrome b 6/f Complexes in Limiting Chloroplast Electron Transport and Determining Photosynthetic Capacity

et al. 2010

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In C 3 plants, CO 2 assimilation is limited by ribulose 1,5-bisphosphate (RuBP) regeneration rate at high CO 2 . RuBP regeneration rate in turn is determined by either the chloroplast electron transport capacity to generate NADPH and ATP or the activity of Calvin cycle enzymes involved in regeneration of RuBP. Here, transgenic tobacco (Nicotiana tabacum 'W38') expressing an antisense gene directed at the transcript of either the Rieske iron-sulfur protein of the cytochrome (Cyt) b 6 /f complex or the d-subunit of chloroplast ATP synthase have been used to investigate the effect of a reduction of these complexes on chloroplast electron transport rate (ETR). Reductions in d-subunit of ATP synthase content did not alter chlorophyll, Cyt b 6 /f complex, or Rubisco content, but reduced ETR estimated either from measurements of chlorophyll fluorescence or CO 2 assimilation rates at high CO 2 . Plants with low ATP synthase content exhibited higher nonphotochemical quenching and achieved higher ETR per ATP synthase than the wild type. The proportional increase in ETR per ATP synthase complex was greatest at 35°C, showing that the ATP synthase activity can vary in vivo. In comparison, there was no difference in the ETR per Cyt b 6 /f complex in plants with reduced Cyt b 6 /f content and the wild type. The ETR decreased more drastically with reductions in Cyt b 6 /f complex than ATP synthase content. This suggests that chloroplast ETR is more limited by Cyt b 6 /f than ATP synthase content and is a potential target for enhancing photosynthetic capacity in crops.Plants capture light energy with their light-harvesting systems, including chlorophylls (Chls) and carotenoids, and drive photosynthetic electron transport through the thylakoid membranes of the chloroplasts. Electrons excised from water in PSII are ultimately transferred to NADP + via PSI, resulting in production of NADPH. This process is known as linear electron transport. At the same time, this linear electron transport that passes through the cytochrome (Cyt) b 6 /f complex generates a proton gradient across the thylakoid membrane (DpH;Allen, 2003). Together with the proton gradient generated by the water-splitting complex associated with PSII, these proton gradients enable ATP production by the ATP synthase complex and help to regulate nonphotochemical quenching (NPQ) of excitation energy (Mü ller et al., 2001). There is also a cyclic electron transport that depends on the PSI photochemical reactions and also passes through the Cyt b 6 /f complex. The cyclic electron transport can generate a DpH and drives ATP synthesis by ATP synthase without concomitant generation of NADPH (Shikanai, 2007). ATP and NADPH generated by light reactions are utilized primarily in the Calvin cycle and photorespiratory cycle. The activity and regulation of the Cyt b 6 /f complex and the ATP synthase are thus key components determining the rate of NADPH and ATP production for CO 2 fixation. Photosynthetic CO 2 assimilation rate can be viewed as being limited either by the capacity o...

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Depletion of stromal P_i induces high ‘energy‐dependent’ antenna exciton quenching (q_E) by decreasing proton conductivity at CF_O‐CF₁ ATP synthase

Cited by 128 publications

References 47 publications

Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase

Feedback limitation of photosynthesis at high CO2 acts by modulating the activity of the chloroplast ATP synthase

Differential expression and phylogenetic analysis suggest specialization of plastid-localized members of the PHT4 phosphate transporter family for photosynthetic and heterotrophic tissues

The Roles of ATP Synthase and the Cytochrome b 6/f Complexes in Limiting Chloroplast Electron Transport and Determining Photosynthetic Capacity

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