Quantitative modeling of energy dissipation in Arabidopsis thaliana

https://doi.org/10.1016/j.envexpbot.2018.03.021Get rights and content

Highlights

  • Structural energy transfer models of photosynthetic pigment-protein complexes.

  • Molecular mechanisms of energy dissipation or quenching in Arabidopsis thaliana.

  • Incorporation of quenching mechanisms into multiscale energy transfer models.

  • Connection between multiscale and regulatory models of quenching.

Abstract

In photosynthesis, solar energy is absorbed and converted into chemical energy. Chlorophyll embedded in proteins absorb light and transfer excitation energy to reaction centers where charge separation occurs. However, the solar flux incident on photosynthetic organisms is highly variable, requiring complex feedback systems to regulate the excitation pressure on reaction centers and prevent excess absorbed energy from causing damage. During periods of transient high light, excess absorbed energy is dissipated as heat. This is routinely observed as the quenching of chlorophyll fluorescence, and often broadly referred to as non-photochemical quenching (NPQ). Understanding the mechanisms through which photosynthetic systems dissipate excess energy and regulate excitation pressure in response to variable light conditions requires extensive quantitative modeling of the photosynthetic system and energy dissipation to interpret experimental observations. This review discusses efforts to model energy dissipation, or quenching, in Arabidopsis thaliana and their connections to models of regulatory systems that control quenching. We begin with a review of theory used to describe energy transfer and experimental data obtained to construct energy transfer models of the photosynthetic antenna system that underlie the interpretation of chlorophyll fluorescence quenching. Second, experimental evidence leading to proposed molecular mechanisms of quenching and the implications for modeling are discussed. The initial incorporation of depictions of proposed mechanisms into quantitative energy transfer models is reviewed. Finally, the necessity of connecting energy transfer models that include molecular models of quenching mechanisms with regulatory models is discussed.

Introduction

Photosynthesis is the process by which organisms absorb sunlight to drive electron transfer and energy storage, but excess sunlight can damage the organism (Blankenship, 2014). The natural fluctuations in light intensity experienced by plants require processes that dissipate energy absorbed in excess of what can be used productively, and that can be rapidly optimized to the light condition (Külheim et al., 2002). Of the two photosystems in higher plants, photoprotection in photosystem II (PSII) has been extensively studied. The suite of dissipative, or photoprotective, mechanisms that protect PSII collectively result in, and are referred to as, non-photochemical quenching (NPQ): the reduction in chlorophyll a fluorescence yield due to dissipation of excess excitation by mechanisms other than photochemistry (Demmig-Adams and Adams, 1992; Niyogi, 1999, Ruban, 2016).

NPQ is a broad term encompassing several constituent components often separated into qE, the rapidly reversible, energy-dependent (pH-dependent) quenching component, and qI, the slowly reversible component associated with PSII photoinhibition (Krause and Weis, 1991; van Kooten and Snel, 1990; Wraight and Crofts, 1970). Although important in many photosynthetic systems, qT, a component of NPQ associated with excitation balance between PSI and PSII by altering the relative antenna size, does not contribute significantly in vascular plants, such as Arabidopsis thaliana, exposed to high light (Niyogi, 1999). qE and another related NPQ component termed qZ (Nilkens et al., 2010) have been the subject of intense study. While there is little consensus surrounding the numerous proposed molecular mechanisms (Duffy and Ruban, 2015) underlying the quenching pathways intrinsic to NPQ in PSII, many elements of the regulation of photoprotection are widely agreed upon (Demmig-Adams et al., 2014). Modeling (Laisk et al., 2009) the proposed mechanisms in the context of the photosynthetic energy transfer network and in the context of the regulatory system provides a powerful way to evaluate whether, and in what way, proposed mechanisms play a role in dissipating energy to protect the photosynthetic solar collection apparatus.

One approach to modeling quenching in the photosynthetic system is to construct a model capable of predicting experimental measurements, including, e.g., of the fluorescence lifetimes of the in vivo system, from quantum and statistical mechanical first principles, structural and spectroscopic data of individual pigments and pigment protein complexes, and membrane imaging (Amarnath et al., 2016). A model must be capable of appropriate treatment of the absorption of light by antenna (Müh et al., 2010, Müh and Renger, 2012, Renger et al., 2011), the transfer of energy to reaction centers (Bennett et al., 2013), and the charge separation process (Novoderezhkin et al., 2011b) to provide a system in which various mechanisms of quenching can be evaluated. Absorption, energy transfer, and charge separation are fundamentally quantum mechanical in their nature. However, to provide a physically meaningful picture, a model must span length scales from angstroms to hundreds of nanometers. To do so requires multiscale modeling and course graining by making appropriate approximations to simplify much of the quantum dynamical calculations; treating the entire system quantum mechanically is impractical, even for modern supercomputers (Kreisbeck and Aspuru-Guzik, 2016). Fortunately, a number of approximations can be made to allow for a model that contains enough of the quantum mechanical features to adequately represent the system. Even so, an accurate model of the system must still integrate data from numerous areas of photosynthesis, making the building of accurate models challenging.

A second area of study that incorporates modeling is the regulatory function of the plant systems that controls the extent of quenching in the photosynthetic antenna (Zaks et al., 2012). The regulatory system operates on timescales from seconds to the lifespan of the plant, but the timescales of greatest interest for regulating the rapid response include changes in the chemical environment of the thylakoid membrane over timescales of seconds to minutes. Current knowledge indicates that a fundamental trigger for inducing quenching is the formation of a transthylakoid pH gradient that, in turn, activates various proteins that influence the actual quenching (Ruban et al., 2012). One of these is the enzyme violaxanthin de-epoxidase that converts violaxanthin to antheraxanthin and zeaxanthin on a timescale of a few minutes when intrathylakoid pH is low (Jahns et al., 2009). These xanthophylls are important players in the molecular mechanisms of quenching and play a number of roles in the pigment protein complexes that effect the ultrafast dynamics of energy transfer. Chemical regulatory models seek to describe quantitatively how the multiple components contribute to the plant system’s regulatory response that controls the quenching.

Important open questions include the importance of various quenching mechanisms identified experimentally, and models of how the biochemical regulatory systems control the activation of potential quenching mechanisms. The dynamic nature of the light incident on plants (Külheim et al., 2002) may imply that various mechanisms could play important roles at different times of day or in different patterns of light variability, suggesting that integrated models of the quenching processes and the regulatory response are key for insight into the potential for optimization (Zhu et al., 2004) of various elements of the quenching mechanisms and regulatory system in order to increase crop yields (Kromdijk et al., 2016) or design biomimetic solar energy devices (Terazono et al., 2011). This review focuses on efforts to model energy dissipation mechanisms using multiscale models that integrate the understanding of structure and function of energy-transfer networks, quenching mechanisms, and chemical regulatory systems that are all necessary for developing the level of understanding and tools required to eventually begin engineering quenching systems.

Section snippets

Models of energy transfer for evaluating quenching mechanisms

Upon absorption of a photon by a chlorophyll molecule in the photosynthetic system, the energy absorbed may be transferred to reaction centers where charge separation occurs that drives down-stream chemical reactions. When reaction centers are unable to productively accept the energy absorbed by antenna chlorophyll, the photosynthetic system must dissipate the excess energy to prevent unwanted generation of reactive oxygen species.

Historically, the flow of energy through the system has been

Mechanistic modeling of quenching

With well-developed models of energy transfer and many of the individual pigment protein complexes parameterized, many of the tools necessary to evaluate mechanistic models of quenching exist. A number of potential mechanisms for the rapidly inducible quenching that protects PSII have been proposed, and it seems likely that no single mechanism dominates the quenching. Broadly, many of the proposed molecular mechanisms involve either interactions between a chlorophyll and a xanthophyll or

Chemical regulation of quenching

In comparison to the controversy surrounding the molecular mechanisms of quenching, there is relative consensus surrounding major components of the biochemical regulatory processes. It is generally accepted that the rapid induction of the quenching response in A. thaliana is triggered by a trans-thylakoid pH gradient that forms in response to high light (Horton et al., 1996) as excitation pressure and charge separation outpace the ATP synthase (Kanazawa and Kramer, 2002). Excessively low pH in

Conclusion

This review discusses the quantitative modeling of energy dissipation, or quenching, in A. thaliana. Starting from energy transfer between individual chlorophyll molecules in the antenna, detailed quantum mechanical treatments are necessary at the fastest timescales. However, as time and length scales increase, much of quantum mechanical detail can be approximated into coarse grained models. These coarse-grained models are useful for evaluating proposed molecular mechanisms of quenching in a

Acknowledgements

We are grateful to Ali Fischer, Soomin Park, Doran I.G. Bennett, and Kapil Amaranth for useful discussions that have informed this approach to the understanding of quenching. This work was supported by US Department of Energy, Office of Science, Basic Energy Sciences, Chemical Sciences, Geosciences, and Biosciences Division Field Work Proposal 449B.

References (154)

  • C. Ilioaia et al.

    Induction of efficient energy dissipation in the isolated light-harvesting complex of Photosystem II in the absence of protein aggregation

    J. Biol. Chem.

    (2008)
  • P. Jahns et al.

    The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II

    Biochim. Biophys. Acta

    (2012)
  • P. Jahns et al.

    Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids

    Biochim. Biophys. Acta

    (2009)
  • S. Jang et al.

    Nonequilibrium generalization of Förster–Dexter theory for excitation energy transfer

    Chem. Phys.

    (2002)
  • W. Kühlbrandt

    Structure of light-harvesting chlorophyll a b protein complex from plant photosynthetic membranes at 7 Å resolution in projection

    J. Mol. Biol.

    (1988)
  • T.P.J. Krüger et al.

    Controlled disorder in plant light-harvesting complex II explains its photoprotective role

    Biophys. J.

    (2012)
  • C. Kreisbeck et al.

    Efficiency of energy funneling in the photosystem II supercomplex of higher plants

    Chem. Sci.

    (2016)
  • S.L.S. Kwa et al.

    Ultrafast energy transfer in LHC-II trimers from the Chl a b light-harvesting antenna of Photosystem II

    Biochim. Biophys. Acta

    (1992)
  • J. Lavorel et al.

    A connected model of the photosynthetic unit

    Biophys. J.

    (1972)
  • X.-P. Li et al.

    Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein

    J. Biol. Chem.

    (2004)
  • N. Liguori et al.

    Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii

    Biochim. Biophys. Acta

    (2016)
  • H. Lokstein et al.

    Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in Photosystem II antenna size and stability

    Biochim. Biophys. Acta

    (2002)
  • F. Müh et al.

    Refined structure-based simulation of plant light-harvesting complex II: Linear optical spectra of trimers and aggregates

    Biochim. Biophys. Acta Bioenerg.

    (2012)
  • Y. Miloslavina et al.

    Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching

    FEBS Lett.

    (2008)
  • M. Nilkens et al.

    Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis

    Biochim. Biophys. Acta

    (2010)
  • G. Paillotin et al.

    Analysis of picosecond laser-induced fluorescence phenomena in photosynthetic membranes using a master equation approach

    Biophys. J.

    (1979)
  • E.İ. İşeri et al.

    Chlorophyll transition dipole moment orientations and pathways for flow of excitation energy among the chlorophylls of the major plant antenna, LHCII

    Eur. Biophys. J.

    (2001)
  • W.W. Adams et al.

    Energy dissipation and photoinhibition: a continuum of photoprotection

    Photoprotection, Photoinhibition, Gene Regulation, and Environment

    (2008)
  • R. Agarwal et al.

    Ultrafast energy transfer in LHC-II revealed by three-pulse photon echo peak shift measurements

    J. Phys. Chem. B

    (2000)
  • T.K. Ahn et al.

    Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein

    Science

    (2008)
  • K. Amarnath et al.

    Multiscale model of light harvesting by photosystem II in plants

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

    (2016)
  • P.W. Atkins et al.

    Molecualr Quantum Mechanics

    (2011)
  • D.I.G. Bennett et al.

    A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes

    J. Am. Chem. Soc.

    (2013)
  • D.I.G. Bennett et al.

    Feedback De-excitation Adjusts the Excitation Diffusion Length to Regulate Photosynthetic Light Harvesting

    (2017)
  • T. Bittner et al.

    Ultrafast excitation energy transfer and exciton-exciton annihilation processes in isolated light harvesting complexes of photosystem II (LHC II) from spinach

    J. Phys. Chem.

    (1994)
  • R.E. Blankenship

    Molecular Mechanisms of Photosynthesis

    (2014)
  • S. Bode et al.

    On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls

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

    (2009)
  • T. Brixner et al.

    Two-dimensional spectroscopy of electronic couplings in photosynthesis

    Nature

    (2005)
  • T.R. Calhoun et al.

    Quantum coherence enabled determination of the energy landscape in light-harvesting complex II

    J. Phys. Chem. B

    (2009)
  • Y.-C. Cheng et al.

    Dynamics of light harvesting in photosynthesis

    Annu. Rev. Phys. Chem.

    (2009)
  • M. Cho et al.

    Exciton analysis in 2D electronic spectroscopy

    J. Phys. Chem. B

    (2005)
  • J.P. Connelly et al.

    Ultrafast spectroscopy of trimeric light-harvesting complex II from higher plants

    J. Phys. Chem. B

    (1997)
  • B. Demmig-Adams et al.

    Photoprotection and other responses of plants to high light stress

    Annu. Rev. Plant Physiol. Plant Micorbial Biol.

    (1992)
  • B. Demmig-Adams et al.

    Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons

    Photosynth. Res.

    (2012)
  • B. Demmig-Adams et al.

    Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria, Photosynthesis and Respiration

    (2014)
  • A. Dreuw et al.

    Charge-transfer state as a possible signature of a zeaxanthin-chlorophyll dimer in the non-photochemical quenching process in green plants

    J. Phys. Chem. B

    (2003)
  • A. Dreuw et al.

    Chlorophyll fluorescence quenching by xanthophylls

    Phys. Chem. Chem. Phys.

    (2003)
  • A. Dreuw et al.

    Role of electron-transfer quenching of chlorophyll fluorescence by carotenoids in non-photochemical quenching of green plants

    Biochem. Soc. Trans.

    (2005)
  • C.D.P. Duffy et al.

    Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII

    J. Phys. Chem. B

    (2013)
  • D.D. Eads et al.

    Direct observation of energy transfer in a photosynthetic membrane: chlorophyll b to chlorophyll a transfer in LHC

    J. Phys. Chem.

    (1989)
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