Regulating the proton budget of higher plant photosynthesis

Avenson, Thomas J.; Cruz, Jeffrey A.; Kanazawa, Atsuko; Kramer, David

doi:10.1073/pnas.0503952102

Cited by 266 publications

(283 citation statements)

References 42 publications

(111 reference statements)

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“…1) as described previously (15,16,25). The extent of the rapid decay of ECS upon switching off actinic light, termed ECS t , which reflects the lightdriven thylakoid pmf was three-to fourfold larger in gamera than in wild type or atpc2 (Fig.…”

Section: Resultsmentioning

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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Section: Resultsmentioning

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 electrochemical potential across thylakoid membranes was assessed using electrochromic shift (ECS)-induced absorbance changes at 520 nm (Avenson et al, 2005;Bailleul et al, 2010;Lucker and Kramer, 2013). When pigments are immobilized within an electric field, a shift in the dipole moment can be induced, which changes the spectral properties of the pigment absorbance.…”

Section: Total Psi Turnover Rate Falls During N Deprivationmentioning

confidence: 99%

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

Deshpande²,

et al. 2014

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The accumulation of carbon storage compounds by many unicellular algae after nutrient deprivation occurs despite declines in their photosynthetic apparatus. To understand the regulation and roles of photosynthesis during this potentially bioenergetically valuable process, we analyzed photosynthetic structure and function after nitrogen deprivation in the model alga Chlamydomonas reinhardtii. Transcriptomic, proteomic, metabolite, and lipid profiling and microscopic time course data were combined with multiple measures of photosynthetic function. Levels of transcripts and proteins of photosystems I and II and most antenna genes fell with differing trajectories; thylakoid membrane lipid levels decreased, while their proportions remained similar and thylakoid membrane organization appeared to be preserved. Cellular chlorophyll (Chl) content decreased more than 2-fold within 24 h, and we conclude from transcript protein and 13 C labeling rates that Chl synthesis was down-regulated both pre-and posttranslationally and that Chl levels fell because of a rapid cessation in synthesis and dilution by cellular growth rather than because of degradation. Photosynthetically driven oxygen production and the efficiency of photosystem II as well as P700 + reduction and electrochromic shift kinetics all decreased over the time course, without evidence of substantial energy overflow. The results also indicate that linear electron flow fell approximately 15% more than cyclic flow over the first 24 h. Comparing Calvin-Benson cycle transcript and enzyme levels with changes in photosynthetic 13 CO 2 incorporation rates also pointed to a coordinated multilevel down-regulation of photosynthetic fluxes during starch synthesis before the induction of high triacylglycerol accumulation rates.

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“…The electron transfer steps are tightly coupled to proton transfer reactions into the thylakoid lumen, storing potential energy in the pmf to drive the synthesis of ATP (8,9). Both NADPH and ATP, in the correct ratios, are required for driving the assimilation of CO 2 and other cellular processes (10).…”

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Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

Davis

Rutherford

Kramer

2017

Phil. Trans. R. Soc. B

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SummaryThere is considerable interest in improving plant productivity by altering the dynamic responses of photosynthesis in tune with natural conditions. This is exemplified by the "energy-dependent" form of nonphotochemical quenching (q E ), the formation and decay of which can be considerably slower than natural light fluctuations, limiting photochemical yield. In addition, we recently reported that rapidly fluctuating light can produce Field Recombination Induced Photodamage (FRIP), where large spikes in electric field across the thylakoid membrane (Δψ) induce photosystem II recombination reactions that produce damaging singlet oxygen ( 1 O 2 ). Both q E and FRIP are directly linked to the thylakoid proton motive force (pmf), and in particular the slow kinetics of partitioning pmf into its ΔpH and Δψ components. Using a series of computational simulations, we explored the possibility of "hacking" pmf partitioning as a target for improving photosynthesis. Under a range of illumination conditions, increasing the rate of counter-ion fluxes across the thylakoid membrane should lead to more rapid dissipation of Δψ and formation of ΔpH. This would result in increased rates for the formation and decay of q E while ameliorating the amplitudes of Δψ-spikes and decreasing 1 O 2 production. These results suggest that ion fluxes may be a viable target for plant breeding or engineering. However, these changes also induce transient, but substantial mismatches in the ATP:NADPH output ratio as well as in the osmotic balance between the lumen and stroma, either of which may explain why evolution has not already accelerated thylakoid ion fluxes. Overall, though the model is simplified, it recapitulates many of the responses seen in vivo, while spotlighting critical aspects of the complex interactions between pmf components and photosynthetic processes. By making the program available, we hope to enable the community of photosynthesis researchers to further explore and test specific hypotheses.*Author for correspondence (kramerd8@cns.msu.edu). 2This opinion/hypothesis paper was inspired by the recent Royal Society symposium on "Enhancing Photosynthesis in Crop Plants: Targets for Improvement," (http://www.rsc.org/events/download/Document/cee7d4f2-9ff1-477b-b155-3e2492577d77) that brought together experts in a range of photosynthetic processes. A prominent theme of several of the presentations was the sensitivity of photosynthesis to rapid, rather than gradual, changes in environmental conditions. Of particular interest was the kinetic mismatch between fluctuations in photosynthetically active radiation (PAR), which can change by orders of magnitude within a second, and the relatively slow onset of photoprotective mechanisms (1, 2). Indeed, there is growing evidence that this mismatch can sensitize both PSI and PSII to oxidative photodamage (3, 4), of which the focus of this paper is the irreversible damage to PSII (to D1 and other subunits) due to 1 O 2 generated by PSII charge recombination. It has also been proposed that the...

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Regulating the proton budget of higher plant photosynthesis

Cited by 266 publications

References 42 publications

Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions

Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

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