Dissipation of Light Energy Absorbed in Excess: The Molecular Mechanisms

2021 ◽  
Vol 72 (1) ◽  
pp. 47-76
Author(s):  
Roberto Bassi ◽  
Luca Dall'Osto

Light is essential for photosynthesis. Nevertheless, its intensity widely changes depending on time of day, weather, season, and localization of individual leaves within canopies. This variability means that light collected by the light-harvesting system is often in excess with respect to photon fluence or spectral quality in the context of the capacity of photosynthetic metabolism to use ATP and reductants produced from the light reactions. Absorption of excess light can lead to increased production of excited, highly reactive intermediates, which expose photosynthetic organisms to serious risks of oxidative damage. Prevention and management of such stress are performed by photoprotective mechanisms, which operate by cutting down light absorption, limiting the generation of redox-active molecules, or scavenging reactive oxygen species that are released despite the operation of preventive mechanisms. Here, we describe the major physiological and molecular mechanisms of photoprotection involved in the harmless removal of the excess light energy absorbed by green algae and land plants. In vivo analyses of mutants targeting photosynthetic components and the enhanced resolution of spectroscopic techniques have highlighted specific mechanisms protecting the photosynthetic apparatus from overexcitation. Recent findings unveil a network of multiple interacting elements, the reaction times of which vary from a millisecond to weeks, that continuously maintain photosynthetic organisms within the narrow safety range between efficient light harvesting and photoprotection.

2016 ◽  
Vol 43 (5) ◽  
pp. 448 ◽  
Author(s):  
Xiao-Ping Yi ◽  
Ya-Li Zhang ◽  
He-Sheng Yao ◽  
Hong-Hai Luo ◽  
Ling Gou ◽  
...  

To better understand the adaptation mechanisms of the photosynthetic apparatus of cotton plants to water deficit conditions, the influence of water deficit on photosynthesis, chlorophyll a fluorescence and the activities of antioxidant systems were determined simultaneously in Gossypium hirsutum L. cv. Xinluzao 45 (upland cotton) and Gossypium barbadense L. cv. Xinhai 21 (pima cotton). Water deficit decreased photosynthesis in both cotton species, but did not decrease chlorophyll content or induce any sustained photoinhibition in either cotton species. Water deficit increased ETR/4 − AG, where ETR/4 estimates the linear photosynthetic electron flux and AG is the gross rate of carbon assimilation. The increase in ETR/4 − AG, which represents an increase in photorespiration and alternative electron fluxes, was particularly pronounced in Xinluzao 45. In Xinluzao 45, water deficit increased the activities of antioxidative enzymes, as well as the contents of reactive oxygen species (ROS), which are related to the Mehler reaction. In contrast, moderate water deficit particularly increased non-photochemical quenching (NPQ) in Xinhai 21. Our results suggest that Xinluzao 45 relied on enhanced electron transport such as photorespiration and the Mehler reaction to dissipate excess light energy under mild and moderate water deficit. Xinhai 21 used enhanced photorespiration for light energy utilisation under mild water deficit but, when subjected to moderate water deficit, possessed a high capacity for dissipating excess light energy via heat dissipation.


2019 ◽  
Author(s):  
Yuval Kolodny ◽  
Hagit Zer ◽  
Mor Propper ◽  
Shira Yochelis ◽  
Yossi Paltiel ◽  
...  

AbstractPhotosynthetic organisms regulate energy transfer to fit to changes in environmental conditions. The biophysical principles underlying the flexibility and efficiency of energy transfer in the light-harvesting process are still not fully understood. Here we examine how energy transfer is regulatedin-vivo. We compare different acclimation states of the photosynthetic apparatus in a marine cyanobacterial species that is well adapted to vertical mixing of the ocean water column and identify a novel acclimation strategy for photosynthetic life under low light intensities. Antennae rods extend, as expected, increasing light absorption. Surprisingly, in contrast to what was known for plants and predicted by classic calculations, these longer rods transfer energy fasteri.e.more efficiently. The fluorescence lifetime and emission spectra dependence on temperature, at the range of 4-300K, suggests that energy transfer efficiency is tuned by modifying the energetic coupling strength between antennae pigments.


2020 ◽  
Vol 295 (51) ◽  
pp. 17816-17826
Author(s):  
Mahendra K. Shukla ◽  
Akimasa Watanabe ◽  
Sam Wilson ◽  
Vasco Giovagnetti ◽  
Ece Imam Moustafa ◽  
...  

Nonphotochemical quenching (NPQ) is a mechanism of regulating light harvesting that protects the photosynthetic apparatus from photodamage by dissipating excess absorbed excitation energy as heat. In higher plants, the major light-harvesting antenna complex (LHCII) of photosystem (PS) II is directly involved in NPQ. The aggregation of LHCII is proposed to be involved in quenching. However, the lack of success in isolating native LHCII aggregates has limited the direct interrogation of this process. The isolation of LHCII in its native state from thylakoid membranes has been problematic because of the use of detergent, which tends to dissociate loosely bound proteins, and the abundance of pigment–protein complexes (e.g. PSI and PSII) embedded in the photosynthetic membrane, which hinders the preparation of aggregated LHCII. Here, we used a novel purification method employing detergent and amphipols to entrap LHCII in its natural states. To enrich the photosynthetic membrane with the major LHCII, we used Arabidopsis thaliana plants lacking the PSII minor antenna complexes (NoM), treated with lincomycin to inhibit the synthesis of PSI and PSII core proteins. Using sucrose density gradients, we succeeded in isolating the trimeric and aggregated forms of LHCII antenna. Violaxanthin- and zeaxanthin-enriched complexes were investigated in dark-adapted, NPQ, and dark recovery states. Zeaxanthin-enriched antenna complexes showed the greatest amount of aggregated LHCII. Notably, the amount of aggregated LHCII decreased upon relaxation of NPQ. Employing this novel preparative method, we obtained a direct evidence for the role of in vivo LHCII aggregation in NPQ.


2006 ◽  
Vol 39 (3) ◽  
pp. 227-324 ◽  
Author(s):  
Richard J. Cogdell ◽  
Andrew Gall ◽  
Jürgen Köhler

1. Introduction 2292. Structures 2342.1 The structure of LH2 2342.2 Natural variants of peripheral antenna complexes 2422.3 RC–LH1 complexes 2423. Spectroscopy 2493.1 Steady-state spectroscopy 2493.2 Factors which affect the position of the Qy absorption band of Bchla 2494. Regulation of biosynthesis and assembly 2574.1 Regulation 2574.1.1 Oxygen 2574.1.2 Light 2584.1.2.1 AppA: blue-light-mediated regulation 2594.1.2.2 Bacteriophytochromes 2594.1.3 From the RC to the mature PSU 2614.2 Assembly 2614.2.1 LH1 2624.2.2 LH2 2635. Frenkel excitons 2655.1 General 2655.2 B800 2675.3 B850 2675.4 B850 delocalization 2736. Energy-transfer pathways: experimental results 2746.1 Theoretical background 2746.2 ‘Follow the excitation energy’ 2766.2.1 Bchla→Bchla energy transfer 2776.2.1.1 B800→B800 2776.2.1.2 B800→B850 2786.2.1.3 B850→B850 2796.2.1.4 B850→B875 2806.2.1.5 B875→RC 2806.2.2 Car[harr ]Bchla energy transfer 2817. Single-molecule spectroscopy 2847.1 Introduction to single-molecule spectroscopy 2847.2 Single-molecule spectroscopy on LH2 2857.2.1 Overview 2857.2.2 B800 2867.2.2.1 General 2867.2.2.2 Intra- and intercomplex disorder of site energies 2877.2.2.3 Electron-phonon coupling 2897.2.2.4 B800→B800 energy transfer revisited 2907.2.3 B850 2938. Quantum mechanics and the purple bacteria LH system 2989. Appendix 2999.1 A crash course on quantum mechanics 2999.2 Interacting dimers 30510. Acknowledgements 30611. References 307This review describes the structures of the two major integral membrane pigment complexes, the RC–LH1 ‘core’ and LH2 complexes, which together make up the light-harvesting system present in typical purple photosynthetic bacteria. The antenna complexes serve to absorb incident solar radiation and to transfer it to the reaction centres, where it is used to ‘power’ the photosynthetic redox reaction and ultimately leads to the synthesis of ATP. Our current understanding of the biosynthesis and assembly of the LH and RC complexes is described, with special emphasis on the roles of the newly described bacteriophytochromes. Using both the structural information and that obtained from a wide variety of biophysical techniques, the details of each of the different energy-transfer reactions that occur, between the absorption of a photon and the charge separation in the RC, are described. Special emphasis is given to show how the use of single-molecule spectroscopy has provided a more detailed understanding of the molecular mechanisms involved in the energy-transfer processes. We have tried, with the help of an Appendix, to make the details of the quantum mechanics that are required to appreciate these molecular mechanisms, accessible to mathematically illiterate biologists. The elegance of the purple bacterial light-harvesting system lies in the way in which it has cleverly exploited quantum mechanics.


2021 ◽  
Author(s):  
Petra Redekop ◽  
Emanuel Sanz-Luque ◽  
Yizhong Yuan ◽  
Gaelle Villain ◽  
Dimitris Petroutsos ◽  
...  

In nature, photosynthetic organisms are exposed to different light spectra and intensities depending on the time of day and atmospheric and environmental conditions. When photosynthetic cells absorb excess light, they induce non-photochemical quenching to avoid photo-damage and trigger expression of photoprotective genes. In this work, we used the green alga Chlamydomonas reinhardtii to assess the impact of light intensity, light quality, wavelength, photosynthetic electron transport and CO2 on induction of the photoprotective genes (LHCSR1, LHCSR3 and PSBS) during dark-to-light transitions. Induction (mRNA accumulation) occurred at very low light intensity, was independently modulated by blue and UV-B radiation through specific photoreceptors, and only LHCSR3 was strongly controlled by CO2 levels through a putative enhancer function of CIA5, a transcription factor that controls genes of the carbon concentrating mechanism. We propose a model that integrates inputs of independent signaling pathways and how they may help the cells anticipate diel conditions and survive in a dynamic light environment.


2003 ◽  
Vol 17 (10) ◽  
pp. 2084-2095 ◽  
Author(s):  
Michael J. Bailey ◽  
Phillip D. Beremand ◽  
Rick Hammer ◽  
Deborah Bell-Pedersen ◽  
Terry L. Thomas ◽  
...  

Abstract The avian pineal gland contains both circadian oscillators and photoreceptors to produce rhythms in biosynthesis of the hormone melatonin in vivo and in vitro. The molecular mechanisms for melatonin biosynthesis are largely understood, but the mechanisms driving the rhythm itself or the photoreceptive processes that entrain the rhythm are unknown. We have produced cDNA microarrays of pineal gland transcripts under light-dark and constant darkness conditions. Rhythmic transcripts were classified according to function, representing diverse functional groups, including phototransduction pathways, transcription/translation factors, ion channel proteins, cell signaling molecules, and immune function genes. These were also organized relative to time of day mRNA abundance in light-dark and constant darkness. The transcriptional profile of the chick pineal gland reveals a more complex form of gene regulation than one might expect from a gland whose sole apparent function is the rhythmic biosynthesis of melatonin. The mRNAs encoding melatonin biosynthesis are rhythmic as are many orthologs of mammalian “clock genes.” However, the oscillation of phototransductive, immune, stress response, hormone binding, and other important processes in the transcriptome of the pineal gland, raises new questions regarding the role of the pineal gland in circadian rhythm generation, organization, and avian physiology.


Forests ◽  
2019 ◽  
Vol 10 (4) ◽  
pp. 312 ◽  
Author(s):  
Yue Wang ◽  
Weiwei Jin ◽  
Yanhui Che ◽  
Dan Huang ◽  
Jiechen Wang ◽  
...  

Nitrogen dioxide (NO2) is recognized as a toxic gaseous air pollutant. However, atmospheric NO2 can be absorbed by plant leaves and subsequently participate in plant nitrogen metabolism. The metabolism of atmospheric NO2 utilizes and consumes the light energy that leaves absorb. As such, it remains unclear whether the consumption of photosynthetic energy through nitrogen metabolism can decrease the photosynthetic capacity of plant leaves or not. In this study, we fumigated mulberry (Morus alba L.) plants with 4 μL·L−1 NO2 and analyzed the distribution of light energy absorbed by plants in NO2 metabolism using gas exchange and chlorophyll a fluorescence technology, as well as biochemical methods. NO2 fumigation enhanced the nitrogen metabolism of mulberry leaves, improved the photorespiration rate, and consumed excess light energy to protect the photosynthetic apparatus. Additionally, the excess light energy absorbed by the photosystem II reaction center in leaves of mulberry was dissipated in the form of heat dissipation. Thus, light energy was absorbed more efficiently in photosynthetic carbon assimilation in mulberry plants fumigated with 4 μL·L−1 NO2, which in turn increased the photosynthetic efficiency of mulberry leaves.


2019 ◽  
Vol 116 (17) ◽  
pp. 8320-8325 ◽  
Author(s):  
Lijin Tian ◽  
Wojciech J. Nawrocki ◽  
Xin Liu ◽  
Iryna Polukhina ◽  
Ivo H. M. van Stokkum ◽  
...  

Sunlight drives photosynthesis but can also cause photodamage. To protect themselves, photosynthetic organisms dissipate the excess absorbed energy as heat, in a process known as nonphotochemical quenching (NPQ). In green algae, diatoms, and mosses, NPQ depends on the light-harvesting complex stress-related (LHCSR) proteins. Here we investigated NPQ inChlamydomonas reinhardtiiusing an approach that maintains the cells in a stable quenched state. We show that in the presence of LHCSR3, all of the photosystem (PS) II complexes are quenched and the LHCs are the site of quenching, which occurs at a rate of ∼150 ps−1and is not induced by LHCII aggregation. The effective light-harvesting capacity of PSII decreases upon NPQ, and the NPQ rate is independent of the redox state of the reaction center. Finally, we could measure the pH dependence of NPQ, showing that the luminal pH is always above 5.5 in vivo and highlighting the role of LHCSR3 as an ultrasensitive pH sensor.


2013 ◽  
Vol 17 (01n02) ◽  
pp. 1-15 ◽  
Author(s):  
Min Chen ◽  
Hugo Scheer

Photosynthetic organisms provide, directly or indirectly, the energy that sustains life on earth by harvesting light from the sun. The amount of light impinging on the surface of the earth vastly surpasses the energy needs of life including man. Harvesting the sun is, therefore, an option for a sustainable energy source: directly by improving biomass production, indirectly by coupling it to the production of hydrogen for fuel or, conceptually, by using photosynthetic strategies for technological solutions based on non-biological or hybrid materials. In this review, we summarize the various light climates on earth, the primary reactions responsible for light harvesting and transduction to chemical energy in photosynthesis, and the mechanisms of competitively adapting the photosynthetic apparatus to the ever-changing light conditions. The focus is on oxygenic photosynthesis, its adaptation to the various light-climates by specialized pigments and on the extension of its limits by the evolution of red-shifted chlorophylls. The implications for potential technical solutions are briefly discussed.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Julianne M Troiano ◽  
Federico Perozeni ◽  
Raymundo Moya ◽  
Luca Zuliani ◽  
Kwangyrul Baek ◽  
...  

Under high light, oxygenic photosynthetic organisms avoid photodamage by thermally dissipating absorbed energy, which is called nonphotochemical quenching. In green algae, a chlorophyll and carotenoid-binding protein, light-harvesting complex stress-related (LHCSR3), detects excess energy via a pH drop and serves as a quenching site. Using a combined in vivo and in vitro approach, we investigated quenching within LHCSR3 from Chlamydomonas reinhardtii. In vitro two distinct quenching processes, individually controlled by pH and zeaxanthin, were identified within LHCSR3. The pH-dependent quenching was removed within a mutant LHCSR3 that lacks the residues that are protonated to sense the pH drop. Observation of quenching in zeaxanthin-enriched LHCSR3 even at neutral pH demonstrated zeaxanthin-dependent quenching, which also occurs in other light-harvesting complexes. Either pH- or zeaxanthin-dependent quenching prevented the formation of damaging reactive oxygen species, and thus the two quenching processes may together provide different induction and recovery kinetics for photoprotection in a changing environment.


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