Modulation of energy-dependent quenching of excitons in antennae of higher plants

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

doi:10.1073/pnas.0401269101

Cited by 134 publications

(221 citation statements)

References 68 publications

(121 reference statements)

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“…While this hypothesis fits with the data reported here in Chlamydomonas, at present no reports for the existence of such activity have been published with plants. Therefore, its possible involvement in the modulation of the parsing of the ∆µ H + , which has been reported in tobacco leaves (56), remains to be investigated.…”

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

confidence: 98%

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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: 98%

“…These conditions further enhance the ability of plants to establish nonphotochemical quenching, although the overall rate of electron flow is drastically reduced (56). The mechanism leading to this different parsing under conditions of inhibited electron flow is not fully understood.…”

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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“…The generation of pmf is likewise coupled to LEF, so it is clear that the sensitivity of antenna regulation (or q E ) must also be modulated in some way to avoid catastrophic failure of photoprotection (12,15,(17)(18)(19). Longer-term acclimation of the q E response can involve altering the sensitivity of the regulatory machinery to lumen pH by changing the xanthophyll pigment and͞or PsbS levels (12, 20).…”

Section: A Need For Flexibility In the Light Reactionsmentioning

confidence: 99%

“…This phenomenon is thought to be achieved by varying either the conductivity of the CF1-CF0 ATP synthase to proton efflux as measured by electrochromic shift (ECS) decay (g H ϩ ), i.e., the inverse of the resistance to proton efflux from the lumen or the relative fraction of pmf stored as ⌬pH (12,(16)(17)(18)24).…”

Section: Two Types Of Flexibility Mechanismsmentioning

confidence: 99%

“…LEF alone is probably unable to satisfy the variable ATP͞NADPH output ratios required to power the sum of the Calvin-Benson cycle (13,14) and other metabolic processes (alternate electron and ATP sinks) that are variably engaged under different physiological conditions (12,15,16). Failure to match ATP͞NADPH output with demand will lead to buildup of products and depletion of substrates for the light reactions, leading to inhibition of the entire process.The generation of pmf is likewise coupled to LEF, so it is clear that the sensitivity of antenna regulation (or q E ) must also be modulated in some way to avoid catastrophic failure of photoprotection (12,15,(17)(18)(19). Longer-term acclimation of the q E response can involve altering the sensitivity of the regulatory machinery to lumen pH by changing the xanthophyll pigment and͞or PsbS levels (12, 20).…”

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Regulating the proton budget of higher plant photosynthesis

Avenson

Cruz

Kanazawa

et al. 2005

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

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In higher plant chloroplasts, transthylakoid proton motive force serves both to drive the synthesis of ATP and to regulate light capture by the photosynthetic antenna to prevent photodamage. In vivo probes of the proton circuit in wild-type and a mutant strain of Arabidopsis thaliana show that regulation of light capture is modulated primarily by altering the resistance of proton efflux from the thylakoid lumen, whereas modulation of proton influx through cyclic electron flow around photosystem I is suggested to play a role in regulating the ATP͞NADPH output ratio of the light reactions.ATP synthase proton conductivity ͉ cyclic electron flow ͉ linear electron flow ͉ energy-dependent nonphotochemical quenching ͉ protein motive force P hotosynthesis converts light energy into chemical energy, ultimately powering the vast majority of our ecosystem (1). Higher plant photosynthesis is initiated through absorption of light by antennae complexes that funnel the energy to photosystem (PS) II and I. The photosystems operate in sequence with the plastoquinone pool, the cytochrome b 6 f complex, and plastocyanin to oxidize H 2 O and reduce NADP ϩ to NADPH in what is termed linear electron flow (LEF). LEF is coupled to proton translocation, establishing a transthylakoid electrochemical gradient of protons, termed the proton motive force (pmf ) (2), comprised of electric field (⌬ ) and pH (⌬pH) gradients (3). Dual Role of the pmfThe pmf plays two central roles in higher plant photosynthesis (4). First, pmf drives the normally endergonic synthesis of ATP through the CF 1 -CF 0 ATP synthase (ATP synthase) (5). Both the ⌬pH and ⌬ components of pmf contribute to ATP synthesis in a thermodynamically, and probably kinetically, equivalent fashion (6). Second, pmf is a key signal for initiating photoprotection of the photosynthetic reaction centers through energydependent nonphotochemical quenching (q E ), a process that harmlessly dissipates excessively absorbed light energy as heat (7-10). Only the ⌬pH component of pmf, through acidification of the lumen, is effective in initiating q E by activating violaxanthin de-epoxidase, a lumen-localized enzyme that converts violaxanthin to antheraxanthin and zeaxanthin, and by protonating lumen-exposed residues of PsbS, a pigment-binding protein of the PS II antenna complex (11). A Need for Flexibility in the Light ReactionsA major open question concerns how the light reactions achieve the flexibility required to meet regulatory needs and match downstream biochemical demands (12). In LEF to NADP ϩ , the synthesis of ATP and the production of NADPH are coupled, producing a fixed ATP͞NADPH output ratio. LEF alone is probably unable to satisfy the variable ATP͞NADPH output ratios required to power the sum of the Calvin-Benson cycle (13,14) and other metabolic processes (alternate electron and ATP sinks) that are variably engaged under different physiological conditions (12,15,16). Failure to match ATP͞NADPH output with demand will lead to buildup of products and depletion of substrates for the...

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Fresh perspectives on an established technique: Pulsed amplitude modulation chlorophyll a fluorescence

Zuo

Aiken

Feng

et al. 2022

Plant Enviro Interactions

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Pulsed amplitude modulation (PAM) chlorophyll a fluorescence provides information about photosynthetic energy transduction. When reliably measured, chlorophyll a fluorescence provides detailed information about critical in vivo photosynthetic processes. Such information has recently provided novel and critical insights into how the yield potential of crops can be improved and it is being used to understand remotely sensed fluorescence, which is termed solar-induced fluorescence and will be solely measured by a satellite scheduled to be launched this year. While PAM chlorophyll a fluorometers measure fluorescence intensity per se, herein we articulate the axiomatic criteria by which instrumentally detected intensities can be assumed to assess fluorescence yield, a phenomenon quite different than fluorescence intensity and one that provides critical insight about how solar energy is variably partitioned into the biosphere. An integrated mathematical, phenomenological, and practical discussion of many useful chlorophyll a fluorescence parameters is presented. We draw attention to, and provide examples of, potential uncertainties that can result from incorrect methodological practices and potentially problematic instrumental design features. Fundamentals of fluorescence measurements are discussed, including the major assumptions underlying the signals and the methodological caveats about taking measurements during both dark-and light-adapted conditions. Key fluorescence parameters are discussed in the context of recent applications under environmental stress. Nuanced information that can be gleaned from intra-comparisons of fluorescence-derived parameters and intercomparisons of fluorescence-derived parameters with those based on other techniques is elucidated.

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Modulation of energy-dependent quenching of excitons in antennae of higher plants

Cited by 134 publications

References 68 publications

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas reinhardtii

Nonphotochemical Quenching of Chlorophyll Fluorescence inChlamydomonas reinhardtii

Regulating the proton budget of higher plant photosynthesis

Fresh perspectives on an established technique: Pulsed amplitude modulation chlorophyll a fluorescence

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