Quantitative modeling of energy dissipation in Arabidopsis thaliana
Graphical abstract
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)
- et al.
Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna
J. Biol. Chem.
(2008) - et al.
Lutein can act as a switchable charge transfer quencher in the CP26 light-harvesting complex
J. Biol. Chem.
(2009) - et al.
Theories for kinetics and yields of fluorescence and photochemistry: how, if at all, can different models of antenna organization be distinguished experimentally?
Biochim. Biophys. Acta
(1999) - et al.
Femtosecond transient absorption spectroscopy on the light-harvesting Chl a/b protein complex of Photosystem II at room temperature and 12 K
Chem. Phys.
(1995) - et al.
The photosystem II subunit S under stress
Biophys. J.
(2017) - et al.
Trapping, loss and annihilation of excitations in a photosynthetic system. I. Theoretical aspects
Biochim. Biophys. Acta Bioenerg.
(1983) - et al.
Dissipative pathways in the photosystem-II antenna in plants
J. Photochem. Photobiol. B: Biol.
(2015) - et al.
The flow of excitation energy in LHCII monomers: implications for the structural model of the major plant antenna
Biophys. J.
(1998) - et al.
Time-dependent density functional theory within the Tamm–Dancoff approximation
Chem. Phys. Lett.
(1999) - et al.
Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll–protein complex
FEBS Lett.
(1991)
Induction of efficient energy dissipation in the isolated light-harvesting complex of Photosystem II in the absence of protein aggregation
J. Biol. Chem.
The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II
Biochim. Biophys. Acta
Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids
Biochim. Biophys. Acta
Nonequilibrium generalization of Förster–Dexter theory for excitation energy transfer
Chem. Phys.
Structure of light-harvesting chlorophyll a b protein complex from plant photosynthetic membranes at 7 Å resolution in projection
J. Mol. Biol.
Controlled disorder in plant light-harvesting complex II explains its photoprotective role
Biophys. J.
Efficiency of energy funneling in the photosystem II supercomplex of higher plants
Chem. Sci.
Ultrafast energy transfer in LHC-II trimers from the Chl a b light-harvesting antenna of Photosystem II
Biochim. Biophys. Acta
A connected model of the photosynthetic unit
Biophys. J.
Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein
J. Biol. Chem.
Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii
Biochim. Biophys. Acta
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
Refined structure-based simulation of plant light-harvesting complex II: Linear optical spectra of trimers and aggregates
Biochim. Biophys. Acta Bioenerg.
Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching
FEBS Lett.
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
Analysis of picosecond laser-induced fluorescence phenomena in photosynthetic membranes using a master equation approach
Biophys. J.
Chlorophyll transition dipole moment orientations and pathways for flow of excitation energy among the chlorophylls of the major plant antenna, LHCII
Eur. Biophys. J.
Energy dissipation and photoinhibition: a continuum of photoprotection
Photoprotection, Photoinhibition, Gene Regulation, and Environment
Ultrafast energy transfer in LHC-II revealed by three-pulse photon echo peak shift measurements
J. Phys. Chem. B
Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein
Science
Multiscale model of light harvesting by photosystem II in plants
Proc. Natl. Acad. Sci. U. S. A.
Molecualr Quantum Mechanics
A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes
J. Am. Chem. Soc.
Feedback De-excitation Adjusts the Excitation Diffusion Length to Regulate Photosynthetic Light Harvesting
Ultrafast excitation energy transfer and exciton-exciton annihilation processes in isolated light harvesting complexes of photosystem II (LHC II) from spinach
J. Phys. Chem.
Molecular Mechanisms of Photosynthesis
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls
Proc. Natl. Acad. Sci. U. S. A.
Two-dimensional spectroscopy of electronic couplings in photosynthesis
Nature
Quantum coherence enabled determination of the energy landscape in light-harvesting complex II
J. Phys. Chem. B
Dynamics of light harvesting in photosynthesis
Annu. Rev. Phys. Chem.
Exciton analysis in 2D electronic spectroscopy
J. Phys. Chem. B
Ultrafast spectroscopy of trimeric light-harvesting complex II from higher plants
J. Phys. Chem. B
Photoprotection and other responses of plants to high light stress
Annu. Rev. Plant Physiol. Plant Micorbial Biol.
Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons
Photosynth. Res.
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria, Photosynthesis and Respiration
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
Chlorophyll fluorescence quenching by xanthophylls
Phys. Chem. Chem. Phys.
Role of electron-transfer quenching of chlorophyll fluorescence by carotenoids in non-photochemical quenching of green plants
Biochem. Soc. Trans.
Modeling of fluorescence quenching by lutein in the plant light-harvesting complex LHCII
J. Phys. Chem. B
Direct observation of energy transfer in a photosynthetic membrane: chlorophyll b to chlorophyll a transfer in LHC
J. Phys. Chem.
Cited by (9)
Electronic and vibrational contributions to the reorganization energy of photosynthetic pigments
2023, Chemical Physics LettersRemote sensing of solar-induced chlorophyll fluorescence (SIF) in vegetation: 50 years of progress
2019, Remote Sensing of EnvironmentCitation Excerpt :These simple models can easily be implemented in canopy-level or global-scale models, but they still rely on empirical coefficients and lack a mechanistic process description of the feedback mechanism. Zaks et al. (2012), Bennett et al. (2018), and Morris and Fleming (2018) developed a dynamic (time-resolved) model that simulates the pools of excited chlorophyll and the concentrations of the quenchers, zeaxanthin and antheraxanthin, using the rate coefficients of the involved processes in a more mechanistic way. Such mechanistic representations could be used in remote sensing models for satellite fluorescence as well.
Photoinhibition or photoprotection of photosynthesis? Update on the (newly termed) sustained quenching component qH
2018, Environmental and Experimental BotanyCitation Excerpt :Simulating excitation energy routes will help tackle these questions that have thus far been addressed using either the lake model (assuming infinite diffusion) or the puddle model (assuming local diffusion). Amarnath et al. (2016) proposed a new model that takes into account the diffusion length of excitation energy as determined by the extent of quenching and thereby improves predictions of fluorescence lifetimes in a given quenching condition; see also Morris and Fleming in the present issue. The expression “too much of a good thing” is often used to refer to photosynthetic organisms' relationship to light.
An integrative approach to photoinhibition and photoprotection of photosynthesis
2018, Environmental and Experimental Botany