Quantifying the roles of algal photosynthetic electron pathways.pdf
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1、Tansley insightQuantifying the roles of algal photosyntheticelectron pathways:a milestone towardsphotosynthetic robustnessAuthor for correspondence:Adrien BurlacotEmail:aburlacotcarnegiescience.eduReceived:31 March 2023Accepted:1 September 2023Adrien Burlacot1,21Department of Plant Biology,Carnegie
2、Institution for Science,Stanford,CA 94305,USA;2Department of Biology,StanfordUniversity,Stanford,CA 94305,USAContentsSummary2197I.Introduction2197II.Molecular mechanisms2199III.Physiological role of alternative electron transport,a quantitative point of view2199IV.Potential of AEFs and conclusions22
3、02Acknowledgements2202References2202New Phytologist(2023)240:21972203doi:10.1111/nph.19328Key words:ecophysiology,microalgae,photoprotection,photosynthesis,photosynthetic electron flows,protongradient.SummaryDuringphotosynthesis,electrontransportreactionsgenerateandshuttlereductanttoallowCO2reductio
4、n by the CalvinBensonBassham cycle and the formation of biomass building block intheso-calledlinearelectronflow(LEF).However,innature,environmentalparameterslikelightintensity or CO2availability can vary and quickly change photosynthesis rates,creating animbalance between photosynthetic energy produ
5、ction and metabolic needs.In addition to LEF,alternative photosynthetic electron flows are central to allow photosynthetic energy to matchmetabolicdemandinresponsetoenvironmentalvariations.Microalgaearguablyharbouroneofthe most diverse set of alternative electron flows(AEFs),including cyclic(CEF),ps
6、eudocyclic(PCEF)and chloroplast-to-mitochondria(CMEF)electron flow.While CEF,PCEF and CMEFhave large functional overlaps,they differ in the conditions they are active and in their role forphotosynthetic energy balance.Here,I review the molecular mechanisms of CEF,PCEF andCMEF in microalgae.I further
7、 propose a quantitative framework to compare their keyphysiological roles and quantify how the photosynthetic energy is partitioned to maintain abalanced energetic status of the cell.Key differences in AEF within the green lineage and thepotential of rewiring photosynthetic electrons to enhance plan
8、t robustness will be discussed.I.IntroductionOn Earth,photosynthesis constitutes the main biological actor oforganic and inorganic carbon cycling on our planet,with thenatural carbon circulation initiated by photosynthetic fixation ofAdrien Burlacot is a finalist of the 2023 New Phytologist Tansley
9、Medalcompetition for excellence in plant science.See Slater&Dolan(2023,240:21712172)for more details.?2023 The AuthorsNew Phytologist?2023 New Phytologist FoundationNew Phytologist(2023)240:ReviewCO2being 10 times larger than the amount of anthropogenicCO2emissions(IPCC,2021),andmicroalgaecontribute
10、tohalfofthis circulation(Field et al.,1998).During photosynthesis,CO2fixation is performed thanks to the combined activity ofphotosystem(PS)IIandI,whichusesunlighttogenerateNADPH(in a so-called linear electron flow LEF)and a trans-thylakoidalproton motive force(pmf)composed of a proton gradient and
11、anelectrical gradient which is used by the ATP synthase to generateATP(Fig.1).Both ATP and NADPH are used by the CalvinBensonBassham(CBB)cycle and the downstream metabolism totransform CO2into biomass building blocks.However,the LEFdoes not generate enough ATP for the requirements of the CBBcycle(Al
12、len,2002)nor for downstream metabolic reactions,andalternative electron flows(AEFs)compensate for this deficiency bygenerating an extra pmf without the net generation of NADPH(Allen,2003).Innaturalhabitats,lightintensity,CO2andnutrientavailability,ortemperaturevary,affectingphotosyntheticrates,theme
13、tabolic demand for energetic vectors or both.An imbalancebetweenmetabolicdemandandphotosyntheticenergyproductioncan cause the accumulation of harmful chemicals like reactiveoxygen species that lead to photo-oxidative damage.In particular,any damage to the PSI is dangerous since PSI recovery requires
14、 thecompletesynthesisofthePSIcomplex,takingdaysforfullrecovery(Bernhard Teicher et al.,2000).The electron transport capacity ofvarious AEF is hence dynamically tuned in response to environ-mental variations,allowing to match metabolic demand for ATPand NADPH without overproduction of energetic vecto
15、rs,thusprotecting the cell from photodamage.Despite their central role,amajorquestionremains:HowmanyelectronsflowingthrougheachAEFareneededtobalancetheenergeticstatusofthecellinresponseto environmental conditions?Here,I review the main alternativeelectron transport pathways in microalgae,their roles
16、 and theH+LumenCytosolChloroplast envelopeATPaseThylakoidPSII H2O O2+1H+2H+2H+H2O1H+O2PCEFCyt b6/fCyt b6/fAFLVsBPSICEF2H+2H+Cyt b6/fPSIPSII2H+2H+PSI*CBBCO2ATPLEFStroma*CMEFvia III/IVMitochondrionAOXATP2H+IIIIIVCMEFvia AOX H2O O2+1H+2H+2H+2H+1H+1H+H2O O2+1H+O2+1H+H2O2.5 H+per e2 H+per e5.5 H+per e3 H
17、+per eCMEF2.5 H+per e in the chloroplastPGR5H+PGRL1Fig.1 Mainalternativeelectronpathwayspresentingreenmicroalgae.Schematicofthephotosyntheticelectrontransportchainwithlinearelectronflow(LEF,brown arrow)generating NADPH(brown stars)and trans-thylakoidal proton(H+)gradient the latter being a component
18、 of the pmf that is used for ATPsynthesis.Both NADPH and ATP are used by the CalvinBensonBassham cycle(CBB)to fix CO2.Cyclic electron flow(CEF,right pink rectangle)andpseudocyclicelectronflow(PCEF,leftpurplerectangle)contributeinthechloroplasttothepmf.Thechloroplast-to-mitochondriaelectronflow(CMEF,
19、topredrectangle)shuttlesreductantusingmultiplemetabolicpathwaysandconvertsitintoATPviaeitherthealternativeoxidase(AOX)pathway(CMEFviaAOX)orthe complex III/IV pathway(CMEF via III/IV).For each electron pathway,the details of theoretical H+translocation reactions occurring per electron(e?)areshownaswe
20、llastheoverallH+translocatedpere?.NoteherethatCMEFtranslocatesH+acrossthethylakoidmembrane(2.5H+pere?,sameforbothCMEFpathways)as well as across the mitochondrial membrane.ATP,adenosine triphosphate;FLVs,flavodiiron proteins A and B;NADPH,reduced form ofnicotinamide adenine dinucleotide phosphate;PS,
21、photosystem;PGR5/L1,proton gradient generation 5/like-1;I,III and IV,complexes I,III and IV of themitochondrial electron transport chain.New Phytologist(2023)240:?2023 The AuthorsNew Phytologist?2023 New Phytologist FoundationReviewTansley insightNewPhytologist2198 14698137,2023,6,Downloaded from ht
22、tps:/ by Xinjiang Branch Of C.A.S,Wiley Online Library on 16/11/2023.See the Terms and Conditions(https:/ Wiley Online Library for rules of use;OA articles are governed by the applicable Creative Commons Licensemolecular mechanisms involved.I then show functional overlapsand key quantitative differe
23、nces of the main AEF mechanisms anduse the model green algae Chlamydomonas reinhardtii(hereafterChlamydomonas)inphotoautotrophic conditionstoillustrate theirvarying roles in response to environmental variations.II.Molecular mechanismsIn Chlamydomonas,three main AEF have been described:cyclic(CEF),ps
24、eudocyclic(PCEF)and chloroplast-to-mitochondria(CMEF)electron flow(Fig.1).The CEF recycles photosyntheticelectrons around PSI and involves two pathways:one regulated bythe proton gradient regulation(PGR)5(Munekage et al.,2002;Johnson et al.,2014)and PGR-Like 1(DalCorso et al.,2008;Tolleter et al.,20
25、11;Fig.1)and another one involving a pathwaydependentonaNADPHdehydrogenase(NDA2)(Janset al.,2008)which reduces plastoquinone directly using NAD(P)H.Because the NDA2-dependent CEF activity likely represents avery small proportion of AEF during photosynthesis(Nawrockiet al.,2019b),this pathway of CEF
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