Most cited article - PubMed ID 29426901
Rate-limiting steps in the dark-to-light transition of Photosystem II - revealed by chlorophyll-a fluorescence induction
The present paper aims to open discussion on the information content, physical mechanism(s), and measuring protocols to determine the partitioning of the absorbed light energy in oxygenic photosynthetic organisms. Revisiting these questions is incited by recent findings discovering that PSII, in addition to its open and closed state, assumes a light-adapted charge-separated state and that chlorophyll a fluorescence induction (ChlF), besides the photochemical activity of PSII, reflects the structural dynamics of its reaction center complex. Thus, the photochemical quantum yield of PSII cannot be determined from the conventional ChlF-based protocol. Consequently, the codependent quantity - the quantum yield of the so-called nonregulatory constitutive nonphotochemical quenching (npq) - loses its physical meaning. Processes beyond photochemistry and regulatory npq should be identified and characterized by multifaceted studies, including ChlF. Such investigations may shed light on the putative roles of dissipation and other energy-consuming events in the stress physiology of photosynthetic machinery.
- Keywords
- Fv/Fm, chlorophyll a fluorescence, constitutive nonregulatory dissipation, nonphotochemical quenching, quantum yield, structural dynamics,
- Publication type
- Journal Article MeSH
In our earlier works, we have shown that the rate-limiting steps, associated with the dark-to-light transition of Photosystem II (PSII), reflecting the photochemical activity and structural dynamics of the reaction center complex, depend largely on the lipidic environment of the protein matrix. Using chlorophyll-a fluorescence transients (ChlF) elicited by single-turnover saturating flashes, it was shown that the half-waiting time (Δτ 1/2) between consecutive excitations, at which 50% of the fluorescence increment was reached, was considerably larger in isolated PSII complexes of Thermostichus (T.) vulcanus than in the native thylakoid membrane (TM). Further, it was shown that the addition of a TM lipid extract shortened Δτ 1/2 of isolated PSII, indicating that at least a fraction of the 'missing' lipid molecules, replaced by detergent molecules, caused the elongation of Δτ 1/2. Here, we performed systematic experiments to obtain information on the nature of TM lipids that are capable of decreasing Δτ 1/2. Our data show that while all lipid species shorten Δτ 1/2, the negatively charged lipid phosphatidylglycerol appears to be the most efficient species - suggesting its prominent role in determining the structural dynamics of PSII reaction center.
- Keywords
- chlorophyll-a fluorescence, core complex of photosystem II, rate-limiting step, structural dynamics, thylakoid lipids, waiting time,
- Publication type
- Journal Article MeSH
Rate-limiting steps in the dark-to-light transition of Photosystem II (PSII) were discovered by measuring the variable chlorophyll-a fluorescence transients elicited by single-turnover saturating flashes (STSFs). It was shown that in diuron-treated samples: (i) the first STSF, despite fully reducing the QA quinone acceptor molecule, generated only an F1(
- Keywords
- chlorophyll-a fluorescence, conformational changes, dielectric relaxation, light-adapted charge-separated state of PSII, rate-limitation, temperature-dependence, waiting time,
- MeSH
- Chlorophyll A MeSH
- Chlorophyll MeSH
- Diuron * pharmacology MeSH
- Photosystem II Protein Complex * MeSH
- Waiting Lists MeSH
- Light MeSH
- Temperature MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Chlorophyll A MeSH
- Chlorophyll MeSH
- Diuron * MeSH
- Photosystem II Protein Complex * MeSH
The purpose of this review is to outline our understanding of the nature, mechanism and physiological significance of light-induced reversible reorganizations in closed Type II reaction centre (RC) complexes. In the so-called 'closed' state, purple bacterial RC (bRC) and photosystem II (PSII) RC complexes are incapable of generating additional stable charge separation. Yet, upon continued excitation they display well-discernible changes in their photophysical and photochemical parameters. Substantial stabilization of their charge-separated states has been thoroughly documented-uncovering light-induced reorganizations in closed RCs and revealing their physiological importance in gradually optimizing the operation of the photosynthetic machinery during the dark-to-light transition. A range of subtle light-induced conformational changes has indeed been detected experimentally in different laboratories using different bRC and PSII-containing preparations. In general, the presently available data strongly suggest similar structural dynamics of closed bRC and PSII RC complexes, and similar physical mechanisms, in which dielectric relaxation processes and structural memory effects of proteins are proposed to play important roles.
- Keywords
- Marcus theory, chlorophyll fluorescence, dielectric relaxation, dynamics and structural memory of proteins, photosystem II, purple bacterial reaction centre,
- MeSH
- Photosynthesis * MeSH
- Photosystem II Protein Complex * metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Review MeSH
- Names of Substances
- Photosystem II Protein Complex * MeSH
Plants growing in nature often experience fluctuating irradiance. However, in the laboratory, the dynamics of photosynthesis are usually explored by instantaneously exposing dark-adapted plants to constant light and examining the dark-to-light transition, which is a poor approximation of natural phenomena. With the aim creating a better approximation, we exposed leaves of pea (Pisum sativum) to oscillating light and measured changes in the functioning of PSI and PSII, and of the proton motive force at the thylakoid membrane. We found that the dynamics depended on the oscillation period, revealing information about the underlying regulatory networks. As demonstrated for a selected oscillation period of 60 s, the regulation tries to keep the reaction centers of PSI and PSII open. We present an evaluation of the data obtained, and discuss the involvement of particular processes in the regulation of photosynthesis. The forced oscillations provided an information-rich fingerprint of complex regulatory networks. We expect future progress in understanding these networks from experiments involving chemical interventions and plant mutants, and by using mathematical modeling and systems identification and control tools.
- Keywords
- Pisum sativum, Fluctuating light, forced oscillations, pea, photosynthesis, photosystem I and II, proton motive force, regulation,
- MeSH
- Photosynthesis physiology MeSH
- Photosystem I Protein Complex metabolism MeSH
- Photosystem II Protein Complex * metabolism MeSH
- Pisum sativum * metabolism MeSH
- Plant Leaves metabolism MeSH
- Plants metabolism MeSH
- Light MeSH
- Electron Transport physiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Photosystem I Protein Complex MeSH
- Photosystem II Protein Complex * MeSH
In our earlier works, we have identified rate-limiting steps in the dark-to-light transition of PSII. By measuring chlorophyll a fluorescence transients elicited by single-turnover saturating flashes (STSFs) we have shown that in diuron-treated samples an STSF generates only F1 (< Fm) fluorescence level, and to produce the maximum (Fm) level, additional excitations are required, which, however, can only be effective if sufficiently long Δτ waiting times are allowed between the excitations. Biological variations in the half-rise time (Δτ 1/2) of the fluorescence increment suggest that it may be sensitive to the physicochemical environment of PSII. Here, we investigated the influence of the lipidic environment on Δτ 1/2 of PSII core complexes of Thermosynechococcus vulcanus. We found that while non-native lipids had no noticeable effects, thylakoid membrane lipids considerably shortened the Δτ 1/2, from ~ 1 ms to ~ 0.2 ms. The importance of the presence of native lipids was confirmed by obtaining similarly short Δτ 1/2 values in the whole T. vulcanus cells and isolated pea thylakoid membranes. Minor, lipid-dependent reorganizations were also observed by steady-state and time-resolved spectroscopic measurements. These data show that the processes beyond the dark-to-light transition of PSII depend significantly on the lipid matrix of the reaction center.
- Keywords
- closed state of PSII, conformational changes, dielectric relaxation, light-adapted state of PSII, light-induced changes, proteoliposomes.,
- Publication type
- Journal Article MeSH
Oxygenic photosynthesis takes place in thylakoid membranes (TM) of cyanobacteria, algae, and higher plants. It begins with light absorption by pigments in large (modular) assemblies of pigment-binding proteins, which then transfer excitation energy to the photosynthetic reaction centers of photosystem (PS) I and PSII. In green algae and plants, these light-harvesting protein complexes contain chlorophylls (Chls) and carotenoids (Cars). However, cyanobacteria, red algae, and glaucophytes contain, in addition, phycobiliproteins in phycobilisomes that are attached to the stromal surface of TM, and transfer excitation energy to the reaction centers via the Chl a molecules in the inner antennas of PSI and PSII. The color and the intensity of the light to which these photosynthetic organisms are exposed in their environment have a great influence on the composition and the structure of the light-harvesting complexes (the antenna) as well as the rest of the photosynthetic apparatus, thus affecting the photosynthetic process and even the entire organism. We present here a perspective on 'Light Quality and Oxygenic Photosynthesis', in memory of George Christos Papageorgiou (9 May 1933-21 November 2020; see notes a and b). Our review includes (1) the influence of the solar spectrum on the antenna composition, and the special significance of Chl a; (2) the effects of light quality on photosynthesis, measured using Chl a fluorescence; and (3) the importance of light quality, intensity, and its duration for the optimal growth of photosynthetic organisms.
