We review the mechanism underlying nonphotochemical chlorophyll fluorescence quenching (NPQ) and its role in protecting plants against photoinhibition. This review includes an introduction to this ...phenomenon, a brief history of major milestones in our understanding of NPQ, definitions, and a discussion of quantitative measurements of NPQ. We discuss the current knowledge and unknown aspects in the NPQ scenario, including the following: ΔpH, the proton gradient (trigger); light-harvesting complex II (LHCII), PSII light harvesting antenna (site); and changes in the antenna induced by ΔpH (change), which lead to the creation of the quencher. We conclude that the minimum requirements for NPQ in vivo are ΔpH, LHCII complexes, and the PsbS protein. We highlight the most important unknown in the NPQ scenario, the mechanism by which PsbS acts upon the LHCII antenna. Finally, we describe a novel, emerging technology for assessing the photoprotective "power" of NPQ and the important findings obtained through this technology
Abstract
Non-photochemical chlorophyll fluorescence quenching (NPQ) remains one of the most studied topics of the 21st century in photosynthesis research. Over the past 30 years, profound knowledge ...has been obtained on the molecular mechanism of NPQ in higher plants. First, the largely overlooked significance of NPQ in protecting the reaction center of photosystem II (RCII) against damage, and the ways to assess its effectiveness are highlighted. Then, the key in vivo signals that can monitor the life of the major NPQ component, qE, are presented. Finally, recent knowledge on the site of qE and the possible molecular events that transmit ΔpH into the conformational change in the major LHCII the major trimeric light harvesting complex of photosystem II (PSII) antenna complex are discussed. Recently, number of reports on Arabidopsis mutants lacking various antenna components of PSII confirmed that the in vivo site of qE rests within the major trimeric LHCII complex. Experiments on biochemistry, spectroscopy, microscopy and molecular modeling suggest an interplay between thylakoid membrane geometry and the dynamics of LHCII, the PsbS (PSII subunit S) protein and thylakoid lipids. The molecular basis for the qE-related conformational change in the thylakoid membrane, including the possible onset of a hydrophobic mismatch between LHCII and lipids, potentiated by PsbS protein, begins to unfold.
In 1991, my colleagues and I published a hypothesis article that proposed a mechanism that controls light harvesting in plants and protects them against photodamage. The major light harvesting ...complex, LHCII, was suggested to undergo aggregation upon exposure of the plant to damaging levels of light. Aggregated LHCII was found to be much less efficient in light harvesting, as it promptly dissipated absorbed energy into heat, possessing a very low chlorophyll fluorescence yield. Nonphotochemical quenching (NPQ) is a term coined to describe this reduction in chlorophyll fluorescence yield. This article is a story of how the hypothesis that LHCII aggregation is involved in NPQ is developed into a model that is now becoming broadly accepted by the research community.
The emergence and evolution of life on our planet was possible because the sun provides energy to our biosphere. Indeed, all life forms need energy for existence and proliferation in space and time. ...Light-energy conversion takes place in photosynthetic organisms that evolve in various environments featuring an impressive range of light intensities that span several orders of magnitude. This property is achieved by the evolution of mechanisms of efficient energy capture that involved development of antenna pigments and pigment–protein complexes as well as the emergence of various strategies on the organismal, cellular, and molecular levels to counteract the detrimental effects of high light intensity on the delicate photosynthetic apparatus. Darwin was one of the first to describe the behaviour of plants towards light. He noticed that some plants try to avoid full day-light and called this reaction paraheliotropism. However, it was only in the second half of the 20th century, when scientists began to discover the structure and molecular mechanisms of the photosynthetic machinery, that the reasons for paraheliotropisms became clear. This review explains the need for the evolution of light adaptations using the example of higher plants. The review focuses on short-term adaptation mechanisms that occur on the minute scale, showing that these processes are fast enough to track rapid fluctuations in light intensity and that they evolved to be effective, allowing for the expansion of plant habitats and promoting diversification and survival. Also introduced are the most recent developments in methods that enable quantification of the light intensities that can be tolerated by plants.
Summary
Photoprotection refers to a set of well defined plant processes that help to prevent the deleterious effects of high and excess light on plant cells, especially within the chloroplast. ...Molecular components of chloroplast photoprotection are closely aligned with those of photosynthesis and together they influence productivity. Proof of principle now exists that major photoprotective processes such as non‐photochemical quenching (NPQ) directly determine whole canopy photosynthesis, biomass and yield via prevention of photoinhibition and a momentary downregulation of photosynthetic quantum yield. However, this phenomenon has neither been quantified nor well characterized across different environments. Here we address this problem by assessing the existing literature with a different approach to that taken previously, beginning with our understanding of the molecular mechanism of NPQ and its regulation within dynamic environments. We then move to the leaf and the plant level, building an understanding of the circumstances (when and where) NPQ limits photosynthesis and linking to our understanding of how this might take place on a molecular and metabolic level. We argue that such approaches are needed to fine tune the relevant features necessary for improving dynamic NPQ in important crop species.
Significance Statement
Photoprotection refers to a diverse set of plant properties that enable the processing of absorbed light energy to efficiently regulate photosynthesis and minimize deleterious reactions caused by excessive energization of pigments. This review explains the way in which the molecular processes of non‐photochemical quenching (a major photoprotective mechanism) act to determine the rate of photosynthesis in dynamic light conditions thus influencing plant productivity, including agricultural yield.
Quantifying the efficiency of photoprotection Ruban, Alexander V.
Philosophical transactions - Royal Society. Biological sciences,
09/2017, Letnik:
372, Številka:
1730
Journal Article
Recenzirano
Odprti dostop
A novel emerging technology for the assessment of the photoprotective ‘power’ of non-photochemical fluorescence quenching (NPQ) has been reviewed and its insightful outcomes are explained using ...several examples. The principles of the method are described in detail as well as the work undertaken for its justification. This pulse amplitude modulated chlorophyll fluorescence approach has been applied for the past 5 years to quantify the photoprotective effectiveness of the NPQ and the light tolerance in Arabidopsis plants grown under various light conditions, during ontogenetic development as well as in a range of mutants impaired in carotenoid and protein biosynthesis. The future applications of this approach for the assessment of crop plant light tolerance are outlined. The perspective of obtaining detailed information about how the extent of photoinhibition and photoprotection can affect plant development, growth and productivity is highlighted, including the potential for us to predict the influence of environmental elements on plant performance and yield of crops. The novel methodology can be used to build up comprehensive light tolerance databases for various current and emerging varieties of crops that are grown outdoors as well as in artificial light environments, in order to optimize for the best environmental conditions that enable high crop productivity.
This article is part of the themed issue ‘Enhancing photosynthesis in crop plants: targets for improvement’.
Under blue light, plant chloroplasts relocate to different areas of the cell. The photoreceptor phototropin2 (phot2) mediates the chloroplast movement mechanism under excess blue light alongside the ...chloroplast unusual positioning1 (chup1) protein. Recently, it has been proposed that leaf transmittance changes associated with chloroplast relocation affect measurements of nonphotochemical quenching (
), resulting in kinetic differences due to these movements (termed "qM"). We evaluated these claims using Arabidopsis (
) knock-out mutants lacking either phot2 or chup1 and analyzed the kinetics of both the onset and recovery of
under equivalent intensities of both red and blue light. We also evaluated the photoprotective ability of chloroplast movements both during the early onset of photoinhibition and under sustained excess light. We monitored photoinhibition using the chlorophyll fluorescence parameter of photochemical quenching in the dark, which measures the redox state of Q
within PSII without any of the complications of traditional
/
measurements. While there were noticeable differences between the responses under red and blue light, the chloroplast movement mechanism had no effect on the rate or amplitude of
onset or recovery. Therefore, we were unable to replicate the "qM" component and its corresponding influence on the kinetics of
in Arabidopsis grown under "shade" conditions. Furthermore, chloroplast relocation had no effect on the high-light tolerance of these plants. These data cast doubt upon the existence of a chloroplast movement-dependent component of
Therefore, the influence of chloroplast movements on photoprotection should be thoroughly reevaluated.
The spring ephemeral Berteroa incana is a familial relative of Arabidopsis thaliana and thrives in a diverse range of terrestrial ecosystems. Within this study, the novel chlorophyll fluorescence ...parameter of photochemical quenching in the dark (qPd) was used to measure the redox state of the primary quinone electron acceptor (QA) in order to estimate the openness of photosystem II (PSII) reaction centres (RC). From this, the early onset of photoinactivation can be sensitively quantified alongside the light tolerance of PSII and the photoprotective efficiency of nonphotochemical quenching (NPQ). This study shows that, with regards to A. thaliana, NPQ is enhanced in B. incana in both low-light (LL) and high-light (HL) acclimation states. Moreover, light tolerance is increased by up to 500%, the rate of photoinactivation is heavily diminished, and the ability to recover from light stress is enhanced in B. incana, relative to A. thaliana. This is due to faster synthesis of zeaxanthin and a larger xanthophyll cycle (XC) pool available for deepoxidation. Moreover, preferential energy transfer via CP47 around the RC further enhances efficient photoprotection. As a result, a high functional cross-section of photosystem II is maintained and is not downregulated when B. incana is acclimated to HL. A greater capacity for protective NPQ allows B. incana to maintain an enhanced light-harvesting capability when acclimated to a range of light conditions. This enhancement of flexible short-term protection saves the metabolic cost of long-term acclimatory changes.
•B. incana displays enhanced NPQ when acclimated to both low and high light.•Light tolerance is increased and photoinhibition is decreased in B. incana.•Zeaxanthin synthesis is upregulated alongside a larger xanthophyll cycle pool.•Energy transfer is preferentially directed via CP47 around the reaction centre.•A large PSII cross-section is maintained across acclimation states in B. incana.
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