Dynamic Changes in Protein-Membrane Association for Regulating Photosynthetic Electron Transport
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cells Review Dynamic Changes in Protein-Membrane Association for Regulating Photosynthetic Electron Transport Marine Messant 1, Anja Krieger-Liszkay 1,* and Ginga Shimakawa 2,3 1 Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Saclay, CEDEX, 91198 Gif-sur-Yvette, France; [email protected] 2 Research Center for Solar Energy Chemistry, Osaka University, 1-3 Machikaneyama, Toyonaka, Osaka 560-8531, Japan; [email protected] 3 Department of Bioscience, School of Biological and Environmental Sciences, Kwansei-Gakuin University, 2-1 Gakuen, Sanda, Hyogo 669-1337, Japan * Correspondence: [email protected] Abstract: Photosynthesis has to work efficiently in contrasting environments such as in shade and full sun. Rapid changes in light intensity and over-reduction of the photosynthetic electron transport chain cause production of reactive oxygen species, which can potentially damage the photosynthetic apparatus. Thus, to avoid such damage, photosynthetic electron transport is regulated on many levels, including light absorption in antenna, electron transfer reactions in the reaction centers, and consumption of ATP and NADPH in different metabolic pathways. Many regulatory mechanisms involve the movement of protein-pigment complexes within the thylakoid membrane. Furthermore, a certain number of chloroplast proteins exist in different oligomerization states, which temporally associate to the thylakoid membrane and modulate their activity. This review Citation: Messant, M.; starts by giving a short overview of the lipid composition of the chloroplast membranes, followed Krieger-Liszkay, A.; Shimakawa, G. by describing supercomplex formation in cyclic electron flow. Protein movements involved in the Dynamic Changes in Protein-Membrane Association for various mechanisms of non-photochemical quenching, including thermal dissipation, state transitions Regulating Photosynthetic Electron and the photosystem II damage–repair cycle are detailed. We highlight the importance of changes Transport. Cells 2021, 10, 1216. in the oligomerization state of VIPP and of the plastid terminal oxidase PTOX and discuss the https://doi.org/10.3390/ factors that may be responsible for these changes. Photosynthesis-related protein movements and cells10051216 organization states of certain proteins all play a role in acclimation of the photosynthetic organism to the environment. Academic Editor: Suleyman Allakhverdiev Keywords: photosynthesis; regulation; abiotic stress; membrane association; thylakoid membrane Received: 13 April 2021 Accepted: 13 May 2021 Published: 16 May 2021 1. Introduction The thylakoid membrane in chloroplasts is a complex three-dimensional structure that Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in is morphologically highly dynamic, as seen by rearrangements of protein complexes under published maps and institutional affil- low light and high light conditions. The thylakoid membrane harbors the photosynthetic iations. electron transport chain. It is known that several processes that regulate the efficiency of light harvesting and electron transport are linked to membrane dynamics. The electron transport chain is made out of the main protein complexes photosystem II (PSII), the site of water oxidation and oxygen release, the cytochrome b6f complex (Cyt b6f ) and photosystem I (PSI), where ferredoxin is reduced. Reduced ferredoxin reduces NADP+ to NADPH, as Copyright: © 2021 by the authors. catalyzed by the Ferredoxin NADP+ oxidoreductase (FNR). Both photosystems contain Licensee MDPI, Basel, Switzerland. This article is an open access article chlorophylls and carotenoids in their reaction centers, in the inner antenna and in the distributed under the terms and light harvesting complexes (LHC). During photosynthetic electron transport, a proton conditions of the Creative Commons gradient (DpH) is established that is, together with an electrochemical gradient (DY), the Attribution (CC BY) license (https:// driving force for the synthesis of ATP by the CF0CF1-ATP synthase. Regulation of light creativecommons.org/licenses/by/ absorption efficiency of the pigment containing antenna systems and of photosynthetic 4.0/). electron transport is essential to allow the plant to acclimate rapidly to changes in light Cells 2021, 10, 1216. https://doi.org/10.3390/cells10051216 https://www.mdpi.com/journal/cells Cells 2021, 10, x FOR PEER REVIEW 2 of 15 Cells 2021, 10, 1216 2 of 15 of light absorption efficiency of the pigment containing antenna systems and of photosyn- thetic electron transport is essential to allow the plant to acclimate rapidly to changes in light intensities, which can occur, for example, in sun flecks, when shade leaves or whole plantsintensities, are suddenly which canexposed occur, to for full example, sun light. in sunRegulation flecks, whenof photosynthetic shade leaves electron or whole transportplants areis also suddenly needed exposed to fulfil tothe full energetic sun light. demands Regulation of the chloroplast/cell/organism of photosynthetic electron bytransport optimizing is alsothe neededATP/NADPH to fulfil ratio. the energetic This can demandsbe achieved of the by chloroplast/cell/organismchanging the activity of cyclicbyoptimizing electron transport the ATP/NADPH around PSI, ratio.a process This requiring can be achievedformation by and changing dissolution the activityof su- percomplexes.of cyclic electron Well transport-characterized around processes PSI, a process involved requiring in the distribution formation andof the dissolution LHCs be- of tweensupercomplexes. the photosystems, Well-characterized the so-called processesstate transitions, involved depend in the on distribution movements of theof large LHCs proteinbetween-pigment the photosystems, complexes within the so-called the membrane. state transitions, Another dependwell-known on movements process that of largein- volvesprotein-pigment protein movements complexes within within the thylakoid the membrane. membrane Another is the well-knownPSII damage– processrepair cy- that cle.involves Furthermore, protein soluble movements proteins within attach the reversibly thylakoid membraneto the thylakoid is the, PSIIenabling damage–repair their in- volvementcycle. Furthermore, in metabolic solublereactions proteins and regulatory attach reversibly mechanisms to the (Figure thylakoid, 1). enabling their involvement in metabolic reactions and regulatory mechanisms (Figure1). FigureFigure 1. Dynamic 1. Dynamic changes changes of the of association the association of proteins of proteins with withthe thylakoid the thylakoid membrane. membrane. In the In the stroma,stroma, proteins proteins can can be present be present in soluble in soluble forms forms or as or peripheral as peripheral membrane membrane proteins, proteins, and their and their oligomerizationoligomerization state state can can change change upon upon membrane membrane association association ( (11).). Transmembrane Transmembrane proteins cancan move movelaterally laterally within within the membranethe membrane and areand associated are associated with differentwith different partner partner proteins proteins (2). Soluble (2). Soluble proteins proteinscan attach can toattach protein to protein complexes complexes in the membrane in the membrane (3). In the (3). lumen, In the solublelumen, soluble proteins proteins can attach can to the attachmembrane to the membrane as a function as ofa function pH (4). of pH (4). InIn this this review, review, we we first first shortly shortly describe describe the the specific specific characteristics characteristics of of the the thylakoid thylakoid membrane.membrane. Then Then,, we we focus focus on oncyclic cyclic electron electron flow, flow, alterations alterations of ofthe the efficiency efficiency of oflight light absorptionabsorption and and dissipation dissipation of excessexcess energy energy as as heat heat (non-photochemical (non-photochemical quenching, quenching NPQ),, NPQfollowed), followed by a by chapter a chapter on state on state transitions transitions and and the the PSII PSII damage–repair damage–repair cycle. cycle. We We will willpresent present other other less less well-known well-known processes processes thatthat are involved in in the the acclimation acclimation response response of ofthe the photosynthetic photosynthetic apparatus apparatus and and which which depend depend on on dynamic dynamic interactions interactions with with the the thylakoidthylakoid membrane membrane (Figure (Figure 2).2 ).We We focus focus mainly mainly on on processes processes taking taking place place in in eukaryotic eukaryotic photosyntheticphotosynthetic organisms. organisms. Cells 2021, 10, 1216 3 of 15 Cells 2021, 10, x FOR PEER REVIEW 3 of 15 Figure 2. DynamicDynamic changes changes of of protein protein–membrane–membrane association association for for regulating regulating photosynthetic photosynthetic electron electron transport. transport. Photosyn- Photo- thetic linear electron flow produces NADPH and ATP for CO2 assimilation in the grana margin. In the grana, heat dissi- synthetic linear electron flow produces NADPH and ATP for CO2 assimilation in the grana margin. In the grana, heat pation at the light-harvesting complex (LHCII), the so-called qE quenching, occurs, and the damaged PSII migrates and is dissipation at the light-harvesting complex (LHCII), the so-called qE quenching, occurs, and the damaged PSII migrates and digested; In the grana margin,