Blanco Nicolás E.

Fusari Corina M.

Gollan Peter J.

Mengin Virginie

Nikkanen Lauri

Frontiers in Plant Science

UTUPub

EDITORIALpublished: 12 April 2022doi: 10.3389/fpls.2022.871623Frontiers in Plant Science | www.frontiersin.org 1 April 2022 | Volume 13 | Article 871623Edited by:Marco Landi,University of Pisa, ItalyReviewed by:Marian Brestic,Slovak University ofAgriculture, SlovakiaLorenzo Ferroni,University of Ferrara, Italy*Correspondence:Nicolás E. Blancoblanco@cefobi-conicet.gov.arPeter J. Gollanpeter.gollan@utu.fiVirginie Menginv.mengin@essex.ac.ukLauri Nikkanenlenikk@utu.fiCorina M. Fusarifusari@cefobi-conicet.gov.arSpecialty section:This article was submitted toPlant Metabolism and Chemodiversity,a section of the journalFrontiers in Plant ScienceReceived: 08 February 2022Accepted: 14 March 2022Published: 12 April 2022Citation:Blanco NE, Gollan PJ, Mengin V,Nikkanen L and Fusari CM (2022)Editorial: A Novel Perspective forPhotosystem I: An Emerging Hub forthe Functional Integration ofPhotosynthesis and Metabolism.Front. Plant Sci. 13:871623.doi: 10.3389/fpls.2022.871623Editorial: A Novel Perspective forPhotosystem I: An Emerging Hub forthe Functional Integration ofPhotosynthesis and MetabolismNicolás E. Blanco 1*, Peter J. Gollan 2*, Virginie Mengin 3*, Lauri Nikkanen 2* andCorina M. Fusari 1*1Centre of Photosynthetic and Biochemical Studies (CEFOBI-CONICET-UNR), Rosario, Argentina, 2Molecular Plant Biology,Department of Life Technologies, University of Turku, Turku, Finland, 3 Schools of Life Sciences, University of Essex,Colchester, United KingdomKeywords: photosystem I, photosynthesis, metabolism, environmental stress, electron transportEditorial on the Research TopicA Novel Perspective for Photosystem I: An Emerging Hub for the Functional Integration ofPhotosynthesis and MetabolismThe autotrophic lifestyle of photosynthetic organisms is determined by their capacity to assimilateCO2 into organic molecules using sunlight as the source of energy. CO2 assimilation providesthe bases to sustain all aspects of plant growth, including division, expansion, function andmaintenance of cells, and production of stress and defense metabolites. Photosynthetic electrontransport (PET) couples absorbed light energy to a chain of redox reactions, leading to formationof a proton motive force and generating NADPH and ATP that are required in the subsequentsteps of CO2 fixation. Behind this definition of photosynthesis, there are multiple complexprocesses associated with the coordination of PET and CO2 assimilation (Stirbet et al., 2020).Energy conversion via photochemical reactions, and gas exchange that facilitates accessibilityand conversion of CO2 to photoassimilates are mutually dependent and directly influencedby environmental conditions (Matuszynska et al., 2019; Walker et al., 2020). Adaptation ofphotosynthesis to external cues has been explored with a focus either on intrinsic aspects ofthe photochemical process (Alric and Johnson, 2017; Tikhonov and Vershubskii, 2017), oron the dynamic of CO2 assimilation via Rubisco carboxylation/oxygenation (Von Caemmerer,2020). Likewise, primary metabolic responses to environmental factors have usually involved thecharacterization of enzymatic activities and central metabolites (e.g., Rubisco, sucrose, starch andprotein biosynthetic pathways), independently of photosynthetic parameters (Stitt et al., 2010).Research on further metabolic processes, such as glycolysis, TCA cycle or lipid metabolism havealso addressed the connection with photosynthesis mostly indirectly, as a downstream proxy ofchanges seen in photosynthetic yield.This Research Topic offered an opportunity to present work investigating simultaneouslyphotosynthesis and primary metabolism from a novel perspective. To encourage moreintegrative research, our proposal was designed to explore photosynthetic energy transductionand CO2 assimilation from photosystem I (PSI) point of view. Recent mounting evidencehas demonstrated that PSI is a critical point in the photosynthetic machinery to respondagainst sudden changes in central metabolism and/or growing conditions. This is in partdue to simultaneous regulatory roles in both upstream photochemical reactions, through thecontrol of photo-protective mechanisms, and downstream metabolic pathways, including CO2fixation and redox levels. Furthermore, the sensitivity of PSI to the imbalance between energyproduction and cell-metabolism demands, a phenomenon called PSI-acceptor side limitation,makes PSI an excellent gauge of non-optimal external conditions (Pollastrini et al., 2020).Blanco et al. Editorial: Back-and-Forth Between Metabolism and PSIIn this Research Topic, the reader can find a set of articlesdemonstrating the intimate connection between centralmetabolism and photosynthetic performance with focus on PSI.The recent advances in the comprehension of the link betweenplastid fatty acid metabolism and redox status are presentedin a mini-review by Hernández and Cejudo. Both the stepsof the biosynthetic pathways for de novo fatty-acid productionand the role of these molecules in photosynthetic performanceand in response to abiotic stress are discussed as part of thechloroplast function. In addition, the authors identified key stepsin lipid metabolism regulated by Thioredoxin (Trx)- NADPH-dependent Trx reductase C (NTRC) at the stroma.The latest findings on the molecular mechanisms of PSIphotoprotection are exposed by Krämer and Kunz. There, theyfocused on the role of the malate valve as a mechanism ofdissipating reducing capacity outside the chloroplast. Their workspotlights not only the stromal NAD(H) as an underappreciatedsource to mitigate PSI damage, but also the activity of twomalate dehydrogenases that explain the generation of NAD(H)in the stroma.Modeling photosynthesis provides a framework to organizeand test hypotheses about specific processes experimentally,revealing targets for engineering photosynthesis. Saadat et al.present an update of the previously published mechanistic modellinking the PET chain with photosynthetic primary metabolism(Matuszynska et al., 2019). This implementation mostly focusedon changing the description of the PSI mechanism from theoriginal model by including reactive oxygen species (ROS)formation and metabolism. Interestingly, it highlighted asignificant impact of Sedoheptulose-1, 7-bisphosphatase onthe regulation of ROS scavenging mechanisms in saturatedCO2 conditions.Ogawa et al. monitored the kinetics of chlorophyll andNADPH fluorescence during photosynthetic induction inorder to elucidate the dynamics between photosynthetic andrespiratory electron transport in the model cyanobacteriumSynechocystis sp. PCC 6803. In cyanobacteria, bothphotosynthetic and respiratory pathways occur on the samethylakoid membranes and share common components suchthe plastoquinone pool, which necessitates strict coordinationof different pathways in order to maintain redox balance invariable environmental conditions. By using mutants deficientin respiratory/cyclic electron transport or the oxidative pentosephosphate pathway, and by studying the effect of glucose as anexogenous electron source, the authors identified the redox stateof the cellular NADPH/NADP+ pool as a key redox sensor at theintersection of photosynthetic and respiratory pathways.The research by Shimakawa et al. investigated distinctpathways of electron donation from PSI to O2 viaphotorespiration or flavodiiron (FLV) protein activity. Bothstrategies achieve oxidation of the P700 reaction center, butare differently utilized during the evolution of photosynthesis.The authors used photosynthetic measurements under standardand low O2 treatments, in wild type and FLV-deficient strainsof the bryophyte Marchantia polymorpha, to show that, whilephotorespiration is active inM. polymorpha, FLV has a dominantrole in P700 oxidation at atmospheric CO2.Finally, Lima-Melo et al. summarized the physiologicalfunction of PSI including its main role as part of PET. Specialattention is placed on the onset of PSI photoinhibition, themultiple mechanisms participating in PSI protection and thelink to stromal sink capacity. Furthermore, ROS productionand associated retrograde signaling pathways are introduced aspart of the response to changes in the equilibrium between PSIinactivation and activity. The authors also introduce a set of openquestions about PSI and provide hints about the direction of theresearch in this topic.At the light of the positive feedback that we received in thisfirst volume of our Research Topic, we are happy to announcethe release of a follow-up issue. With this initiative, we hope tobroaden the scope by reaching out for more studies integratingaspects of photosynthesis and metabolism. Please find more infoat: https://www.frontiersin.org/research-topics/31418/the-back-and-forth-between-metabolism-and-photosystem-i-volume-ii.We are looking forward to your contributions that drivefurther understanding of the rich and complex operation ofphotosynthetic organisms.AUTHOR CONTRIBUTIONSAll authors listed have made a substantial, direct, and intellectualcontribution to the work and approved it for publication.ACKNOWLEDGMENTSNEB and CMF are Researchers of Consejo Nacional deInvestigaciones Científicas y Técnicas (National Council ofScience of Argentina, CONICET), Argentina.REFERENCESAlric, J., and Johnson, X. (2017). Alternative electron transport pathways inphotosynthesis: a confluence of regulation. Curr. Opin. Plant Biol. 37, 78–86.doi: 10.1016/j.pbi.2017.03.014Matuszynska, A., Saadat, N. P., and Ebenhoh, O. (2019). Balancing energy supplyduring photosynthesis - a theoretical perspective. Physiol. Plant. 166, 392–402.doi: 10.1111/ppl.12962Pollastrini, M., Salvatori, E., Fusaro, L., Manes, F., Marzuoli, R., Gerosa, G., etal. (2020). Selection of tree species for forests under climate change: is PSIfunctioning a better predictor for net photosynthesis and growth than PSII?Tree Physiol. 40, 1561–1571. doi: 10.1093/treephys/tpaa084Stirbet, A., Lazar, D., Guo, Y., and Govindjee, G. (2020). Photosynthesis:basics, history and modelling. Ann. Bot. 126, 511–537. doi: 10.1093/aob/mcz171Stitt, M., Lunn, J., and Usadel, B. (2010). Arabidopsis and primary photosyntheticmetabolism – more than the icing on the cake. Plant J. 61, 1067–1091.doi: 10.1111/j.1365-313X.2010.04142.xTikhonov, A. N., and Vershubskii, A. V. (2017). Connectivity between electrontransport complexes and modulation of photosystem II activity in chloroplasts.Photosynth. Res. 133, 103–114. doi: 10.1007/s11120-017-0349-zVon Caemmerer, S. (2020). Rubisco carboxylase/oxygenase: From the enzymeto the globe: A gas exchange perspective. J. Plant Physiol. 252:153240.doi: 10.1016/j.jplph.2020.153240Frontiers in Plant Science | www.frontiersin.org 2 April 2022 | Volume 13 | Article 871623Blanco et al. Editorial: Back-and-Forth Between Metabolism and PSIWalker, B. J., Kramer, D. M., Fisher, N., and Fu, X. (2020). Flexibility in the energybalancing network of photosynthesis enables safe operation under changingenvironmental conditions. Plants (Basel) 9:301. doi: 10.3390/plants9030301Conflict of Interest: The authors declare that the research was conducted in theabsence of any commercial or financial relationships that could be construed as apotential conflict of interest.Publisher’s Note: All claims expressed in this article are solely those of the authorsand do not necessarily represent those of their affiliated organizations, or those ofthe publisher, the editors and the reviewers. Any product that may be evaluated inthis article, or claim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.Copyright © 2022 Blanco, Gollan, Mengin, Nikkanen and Fusari. Thisis an open-access article distributed under the terms of the CreativeCommons Attribution License (CC BY). The use, distribution or reproductionin other forums is permitted, provided the original author(s) and thecopyright owner(s) are credited and that the original publication in thisjournal is cited, in accordance with accepted academic practice. No use,distribution or reproduction is permitted which does not comply with theseterms.Frontiers in Plant Science | www.frontiersin.org 3 April 2022 | Volume 13 | Article 871623

Editorial: A Novel Perspective for Photosystem I: An Emerging Hub for the Functional Integration of Photosynthesis and Metabolism

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Editorial: A Novel Perspective for Photosystem I: An Emerging Hub for the Functional Integration of Photosynthesis and Metabolism

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