Balancing the central roles of the thylakoid proton gradient

Kramer, David; Cruz, Jeffrey A.; Kanazawa, Atsuko

doi:10.1016/s1360-1385(02)00010-9

Cited by 244 publications

(195 citation statements)

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“…The mechanism leading to this different parsing under conditions of inhibited electron flow is not fully understood. It has been argued, however, that changes in the ionic stromal balance, or in the lumenal buffer capacity, are likely to be the major effectors of this phenomenon in plants (49,56,58,59).…”

Section: A Reduced Capacity To Maintain a ∆Ph At Steady State Under Imentioning

confidence: 99%

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas reinhardtii

et al. 2006

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Unlike plants, Chlamydomonas reinhardtii shows a restricted ability to develop nonphotochemical quenching upon illumination. Most of this limited quenching is due to state transitions instead of ∆pH-driven high-energy state quenching, qE. The latter could only be observed when the ability of the cells to perform photosynthesis was impaired, either by lowering temperature to ∼0°C or in mutants lacking RubisCO activity. Two main features were identified that account for the low level of qE in Chlamydomonas. On one hand, the electrochemical proton gradient generated upon illumination is apparently not sufficient to promote fluorescence quenching. On the other hand, the capacity to transduce the presence of a ∆pH into a quenching response is also intrinsically decreased in this alga, when compared to plants. The possible mechanism leading to these differences is discussed.The absorption of light in excess of the capacity for photosynthetic electron transport is damaging to photosynthetic organisms (1). That capacity is, however, variable, depending mainly on the efficiency of CO 2 assimilation. For example, decreases in temperature lower the rate with which electrons can be transported within the electron transport chain as well as the capacity of metabolic processes to assimilate the reductant that has been photoproduced. In higher plants, the availability of CO 2 is liable to be limiting under conditions of water stress, due to the closure of stomata. This will again inhibit photosynthetic assimilation. Under such conditions, cells are likely to experience oxidative stress, due to the uncontrolled formation of reactive oxygen species associated with the absorption of light by chlorophyll.Under conditions of excess light, a variety of mechanisms are initiated which protect chloroplasts from damage. In higher plants, a number of processes have been identified, primarily through application of measurements of chlorophyll fluorescence yield. These are all associated with photosystem (PS) 1 II and are collectively referred to as nonphotochemical quenching mechanisms (NPQ; 1). However, this term comprises at least three processes: (i) qI, mainly related to photoinhibition, a slowly reversible damage to PSII reaction centers (2, 3), although data suggest that a zeaxanthindependent quenching might contribute substantially to this process (4, 5), (ii) qT, state transitions, a change in the relative antenna sizes of PSII and PSI, due to the reversible phosphorylation and migration of antenna proteins (LHCII) (6), and (iii) qE, also termed "high-energy state quenching", a form of quenching associated with the development of a low pH in the thylakoid lumen (e.g., ref 7).High-energy state quenching is largely thought to be associated with an increase in thermal dissipation within the light-harvesting apparatus (1,8,9), associated with the generation of a ∆pH (7, 10) and with the formation of zeaxanthin via deepoxidation of violaxanthin (11). However, in vitro at least, this term also encompasses acidic pHinduced proc...

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Section: A Reduced Capacity To Maintain a ∆Ph At Steady State Under Imentioning

confidence: 99%

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas reinhardtii

et al. 2006

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“…In mitochondria, pmf is held mainly as Δψ, allowing enzymes to operate at optimal 3 pH ranges. In chloroplasts, the build-up of ΔpH results in acidification of the thylakoid lumen, which acts to feedback regulate (or control) critical steps in the light reactions (reviewed in (19)), including: 1) the activation of the photoprotective q E response (through activation of violaxanthin deepoxidase and protonation of PsbS, (11); and 2) "photosynthetic control" of electron flow at the cytochrome b 6 f complex (reviewed in (23) Early work on isolated thylakoids suggested that pmf was stored mainly as ΔpH in thylakoids, but more recent work suggests that a pure ΔpH pmf is incompatible with the known pH dependencies of photosynthetic processes (23,27). A range of in vivo studies (4,19,24,(28)(29)(30)(31)(32) support the view that the pmf is actively partitioned into Δψ and ΔpH components to avoid severe restrictions on b 6 f activity or acid-induced damage to lumenal components, while balancing the needs for efficient energy storage and activation of lumen pH-responsive photoprotective processes (27).…”

mentioning

confidence: 99%

“…There have also been proposals that PSII can be regulated or inhibited (23,25) at low lumen pH, for example by acid-induced release of Ca 2+ from the oxygen evolving complex (OEC), or by limiting electron flow by slowing of the OEC S-state transitions (25,26). Early work on isolated thylakoids suggested that pmf was stored mainly as ΔpH in thylakoids, but more recent work suggests that a pure ΔpH pmf is incompatible with the known pH dependencies of photosynthetic processes (23,27). A range of in vivo studies (4,19,24,(28)(29)(30)(31)(32) support the view that the pmf is actively partitioned into Δψ and ΔpH components to avoid severe restrictions on b 6 f activity or acid-induced damage to lumenal components, while balancing the needs for efficient energy storage and activation of lumen pH-responsive photoprotective processes (27).…”

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confidence: 99%

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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“…pH-dependent dissipation of excess energy in the LHCII to protect the photosynthetic apparatus against photooxidation [12][13][14] ; (iv) "Photosynthesis Control," i.e., regulation of electron transport by the Cyt b 6 f complex, governed by the pH of thylakoid lumen and stroma. [15][16][17][18] In this review, we will describe the interconnections and the relative importance of these photoprotective mechanisms, with a particular focus on photosynthesis control and its role in the pH-dependent control of plastoquinol (PQH 2 ) oxidation at the Qo-site of the Cyt b 6 f complex, which regulates the overall rate of the intersystem electron transport.…”

Section: Introductionmentioning

confidence: 99%

Photosynthesis Control: An underrated short-term regulatory mechanism essential for plant viability

Colombo

Suorsa

Rossi

et al. 2016

Plant Signaling & Behavior

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Regulation of photosynthetic electron transport provides efficient performance of oxygenic photosynthesis in plants. During the last 15 years, the molecular bases of various photosynthesis shortterm regulatory processes have been elucidated, however the wild type-like phenotypes of mutants lacking of State Transitions, Non Photochemical Quenching, or Cyclic Electron Transport, when grown under constant light conditions, have also raised doubts about the acclimatory significance of these shortregulatory mechanisms on plant performance. Interestingly, recent studies performed by growing wild type and mutant plants under field conditions revealed a prominent role of State Transitions and Non Photochemical Quenching on plant fitness, with almost no effect on vegetative plant growth. Conversely, the analysis of plants lacking the regulation of electron transport by the cytochrome b 6 f complex, also known as Photosynthesis Control, revealed the fundamental role of this regulatory mechanism in the survival of young, developing seedlings under fluctuating light conditions.

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Balancing the central roles of the thylakoid proton gradient

Cited by 244 publications

References 24 publications

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas reinhardtii

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas 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

Photosynthesis Control: An underrated short-term regulatory mechanism essential for plant viability

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