Current knowledge on mechanisms preventing photosynthesis redox imbalance in plants

an ioxidan s Re iew Cu en Knowledge on Mechanisms P e en ing Pho osyn hesis Redox Imbalance in Plan s Ma ía-C uz González 1,* , F ancisco Ja ie Cejudo 1, Ma iam Sah awy 2and An onio Jesús Se a o 2,*   Ci a ion: González, M.-C.; Cejudo, F.J.; Sah awy, M.; Se a o, A.J. Cu en Knowledge on Mechanisms P e en ing Pho osyn hesis Redox Imbalance in Plan s. An ioxidan s 2021,10, 1789. h ps://doi.o g/ 10.3390/an iox10111789 Academic Edi o : Michel Ha aux Recei ed: 11 Oc obe 2021 Accep ed: 5 No embe 2021 Published: 9 No embe 2021 Publishe ’s No e: MDPI s ays neu al wi h ega d o ju isdic ional claims in published maps and ins i u ional a il- ia ions. Copy igh : © 2021 by he au ho s. Licensee MDPI, Basel, Swi ze land. This a icle is an open access a icle dis ibu ed unde he e ms and condi ions o he C ea i e Commons A ibu ion (CC BY) license (h ps:// c ea i ecommons.o g/licenses/by/ 4.0/). 1Ins i u o de Bioquímica Vege al y Fo osín esis, Uni e sidad de Se illa-Consejo Supe io de In es igaciones Cien í icas (CSIC), A da. Amé ico Vespucio 49, 41092 Se illa, Spain; [email p o ec ed] 2Depa amen o de Bioquímica, Biología Celula y Molecula de Plan as, Es ación Expe imen al del Zaidín, Consejo Supe io de In es igaciones Cien í icas (CSIC), 18008 G anada, Spain; [email p o ec ed] *Co espondence: [email p o ec ed] (M.-C.G.); [email p o ec ed] (A.J.S.) Abs ac : Pho osyn hesis includes a se o edox eac ions ha a e he sou ce o educing powe and ene gy o he assimila ion o ino ganic ca bon, ni ogen and sulphu , hus gene a ing o ganic compounds, and oxygen, which suppo s li e on Ea h. As sessile o ganisms, plan s ha e o ace con inuous changes in en i onmen al condi ions and need o adjus he pho osyn he ic elec on anspo o p e en he accumula ion o damaging oxygen by-p oduc s. The balance be ween pho osyn he ic cyclic and linea elec on lows allows o he main enance o a p ope NADPH/ATP a io ha is adap ed o he plan ’s needs. In addi ion, di e en mechanisms o dissipa e excess ene gy ope a e in plan s o p o ec and op imise pho osyn hesis unde ad e se condi ions. Recen epo s show an impo an ole o edox-based di hiol–disulphide in e changes, media ed bo h by classical and a ypical chlo oplas hio edoxins (TRXs), in he con ol o hese pho op o ec i e mechanisms. Mo eo e , memb ane-ancho ed TRX-like p o eins, such as HCF164, which ans e elec ons om s omal TRXs o he hylakoid lumen, play a key ole in he egula ion o lumenal a ge s depending on he s omal edox poise. In e es ingly, no all pho op o ec i e playe s we e epo ed o be unde he con ol o TRXs. In his e iew, we discuss ecen indings ega ding he mechanisms ha allow an app op ia e elec on lux o a oid he de imen al consequences o pho osyn hesis edox imbalances. Keywo ds: hio edoxins (TRX); pho osyn hesis; edox; NADPH hio edoxin educ ase C (NTRC); non-pho ochemical quenching (NPQ); cyclic elec on low (CEF); e edoxin/PGR5/PGRL1-dependen plas oquinone educ ase (PGR5/PGRL1); NADH dehyd ogenase-like complex (NDH) 1. In oduc ion Mos o li e on Ea h is sus ained by pho ochemical eac ions. In gene al e ms, in he so-called linea elec on low (LEF), pho osyn he ic ligh eac ions in ol e h ee mul i-p o ein complexes: pho osys ems (PS) II and I, and he cy och ome b 6 (Cy b 6 ) complex [ 1 , 2 ]. PS a e associa ed wi h ligh -ha es ing complexes (LHCs), which a e e- sponsible o sunligh abso p ion in plan s and g een algae [ 3 , 4 ]. LEF s a s wi h he pho o-induced wa e oxida ion ha dona es elec ons o PSII and ends wi h he e edoxin (Fd) educ ion by PSI. Addi ionally, a balancing cyclic elec on low (CEF) wo ks oge he wi h LEF o ine- une he whole pho osyn he ic p ocess [ 5 , 6 ]. CEF depends on addi ional pho osyn he ic complexes: he NADH dehyd ogenase-like (NDH) complex and/o he e edoxin/PROTON GRADIENT REGULATION 5 (PGR5)/PGR5-LIKE PHOTOSYN- THETIC PHENOTYPE 1 (PGRL1) complex. Oxygenic pho osyn hesis p o oked he ise o molecula oxygen (O 2 ) in he a mo- sphe e app oxima ely 2.3–2.4 billion yea s ago [ 7 , 8 ]. Exposi ion o highe le els o O 2 , and i s de i a i e eac i e oxygen species (ROS), led o a massi e ex inc ion e en [ 9 ]. F om hen on, li ing o ganisms ha e aken ad an age o ROS o egula e hei own de elop- men [ 10 , 11 ]. In plan s, bo h enzyma ic and non-enzyma ic sys ems sca enge excess ROS hus p e en ing ROS-de i ed damage o di e en cell componen s, such as DNA, lipids An ioxidan s 2021,10, 1789. h ps://doi.o g/10.3390/an iox10111789 h ps://www.mdpi.com/jou nal/an ioxidan s An ioxidan s 2021,10, 1789 2 o 17 and p o eins [ 12 ]. In chlo oplas s, ROS play a key ole in he pho oinhibi ion o PSII unde high ligh , hinde ing i s epai h ough he inhibi ion o D1 ansla ion [ 13 ]. Howe e , despi e hei po en ially ha m ul e ec s, ROS de i ed om pho osyn hesis [ 14 , 15 ] ha e a ele an ole as signalling molecules o he egula ion o chlo oplas p ocesses wi h an impo an impac on plan de elopmen and acclima ion o en i onmen al s ess [ 11 , 14 – 17 ]. To p ese e plan pe o mance unde ad e se en i onmen al condi ions, he pho- osyn he ic elec on anspo chain (PETC) mus be inely uned acco ding o in e nal and ex e nal signals. Plan pho osyn hesis allows he use o educing equi alen s, gene - a ed by ligh -d i en ex ac ion o elec ons om wa e , o suppo biosyn he ic pa hways, including CO 2 ixa ion o ni ogen assimila ion. In gene al e ms, PETC pe o mance g ea ly depends on a p ope balance be ween abso bed ligh and he me abolic demand o chemical ene gy. Rapid en i onmen al changes can o e low PETC causing he ac- cumula ion o ROS, which may damage he mos sensi i e molecula componen s o he pho osyn he ic machine y [ 13 ]. When edox imbalance occu s in chlo oplas s, o ins ance, due o s ong luc ua ions in ligh in ensi y, p o ec i e mechanisms a e igge ed o p e- se e edox homeos asis. As p e iously men ioned, many o hese mechanisms ely on sca enging o e -accumula ed ROS [ 12 ]. A he same ime, an addi ional s a egy consis s in ebalancing pho osyn hesis o cope wi h un a ou able g ow h condi ions, hus p e en - ing an oxida i e bu s and i s ha m ul ou comes h ough se e al conse ed egula o y mechanisms, which include (i) balancing he NADPH/ATP a io wi h he cyclic elec on low (CEF) ca ied ou by he chlo oplas NADH dehyd ogenase-like (NDH) and he Fd/PGR5/PGRL1-dependen PQ educ ase (PGR5/PGRL1) complexes, (ii) dissipa ing excess ene gy by non-pho ochemical quenching (NPQ), (iii) he appea ance o new quench- ing si es in PSII pe iphe al an enna, (i ) edis ibu ion o exci a ion ene gy h ough s a e ansi ions dependen on he phospho yla ion o LHCII, ( ) speci ic emo al and epai o PSII damaged p o ein componen s, such as D1 and he ex insic p o ein PsbO, and ( i) egula ing he plas oquinone educ ion by he plas id e minal oxidase (PTOX). Pho osyn he ic complexes loca ed a he chlo oplas hylakoid memb ane de ine wo ine- uned in e connec ed sub-compa men s. While in insic p o eins ace bo h he hy- lakoidal lumen and he s oma, ex insic p o eins ace ei he one o ano he side and, consequen ly, hese pho osyn hesis complexes in e ac in synch ony wi hin wo physically sepa a ed p o ein ne wo ks. Rega ding edox poise and pH, he s oma is a mo e educing and basic en i onmen han he hylakoid lumen [ 18 ]. Because sunligh in ensi y is con in- uously changing in na u e, pho osyn hesis con ol (and p o ec ion) la gely elies on as egula o y mechanisms in ol ing edox-based pos - ansla ional modi ica ions (PTMs), which ake place a bo h sides o hylakoid memb anes in a coo dina ed manne [ 19 ]. When p o eins a e exposed o ROS, sul hyd yl g oups (-SH) o Cys esidues can be oxidised o sul enic acid (-SOH) [ 20 ]. The occu ence o ano he Cys nea his g oup can lead o he o ma ion o a co alen in a- o in e molecula disulphide bond [ 21 ]. Usually, his PTM has impo an e ec s on p o ein con o ma ion, ac i i y and e en s abili y, hence becoming a dynamic egula o y mechanism in some p o eins ha can swi ch be ween wo edox s a es ( hiol/disulphide) o o m mul ip o ein complexes [ 22 – 24 ]. Some membe s o he chlo o- plas hio edoxin (TRX) amily we e epo ed o be key playe s in he edox egula ion o ligh -dependen p ocesses [ 25 – 28 ]. TRXs a e edox signalling p o eins wi h an ac i e si e con aining wo Cys sepa a ed by wo amino acid esidues (CXXC). These edox p o eins a e p one o ans e elec ons o a ge p o eins and hei enzyma ic mechanism implies a di hiol/disulphide in e change [ 29 ]. In chlo oplas s, hese p o eins a e educed by he Fd-TRX educ ase (FTR), which ecei es elec ons om pho osyn he ically educed Fds [ 30 ]. Classic TRXs, wi h he conse ed ac i e si e WCG/PPC, o m a mul igenic amily com- posed o di e en ypes ( ,m,x,yand z) [31,32]. In A abidopsis haliana, he - and m- ypes a e he mos abundan TRX iso o ms in he chlo oplas [ 33 ] and pa icipa e in he egula ion o impo an p ocesses such as he Cal in–Benson cycle and he pho osyn hesis ligh eac- ions [ 34 – 36 ]. Chlo oplas non-classic TRXs include a pa icula p o ein named NADPH TRX educ ase C (NTRC), which ecei es educing equi alen s om NADPH [ 37 , 38 ] and An ioxidan s 2021,10, 1789 3 o 17 was p oposed o be a key playe in chlo oplas edox homeos asis [ 39 , 40 ]. In e es ingly, classic TRXs and NTRC a e es ic ed o he chlo oplas s oma, indica ing ha edox egu- la ion is pa icula ly ele an in his chlo oplas compa men in line wi h ecen e iews ha ha e highligh ed he impo ance o edox egula ion o s omal p ocesses [ 34 , 35 , 41 ]. Besides s omal TRXs, lumenal TRX-like coun e pa s, such as HCF164, ancho ed o he hylakoid memb ane, we e iden i ied [ 42 ]. HCF164 can ecei e educing equi alen s om s omal TRXs m h ough he hylakoid-memb ane p o ein CCDA [ 19 , 43 , 44 ]. The e o e, acco ding o he cu en model, he lumenal sys em CCDA/HCF164 depends on he s o- mal FTR/TRX edox sys em. Ne e heless, he in e ela ion be ween s omal and lumenal TRXs in he edox egula ion o ligh eac ions o pho osyn hesis is la gely unknown. As pho osyn hesis can be conside ed he mos impo an biological p ocess o li e on Ea h, he knowledge o he signalling ne wo ks, including edox egula ion, ha ope a es in he con ol o ligh eac ions o pho osyn hesis, is key o unde s anding he li e-adap a ion success on ou plane . Thus, he aim o his e iew is o un eil an in eg a i e iew o he di e en egula o y mechanisms ebalancing pho osyn hesis ligh eac ions unde un a ou able condi ions. In his ega d, TRXs a e key egula o y playe s ecei - ing in o ma ion abou he edox s a e o he PETC, con eying back his in o ma ion o o ches a e he whole pho osyn he ic p ocess. Howe e , o he mechanisms, wi h so a no epo ed TRX-dependen edox egula ion, which pa icipa e in he balance o edox homeos asis in g een issues, will also be discussed. 2. Balancing Pho osyn hesis h ough Cyclic Elec on Flow CEF has e ol ed o di e elec ons back o PETC o enhance H + pumping o boos he p o on mo i e o ce (PMF) ac oss he hylakoid memb anes [ 45 ]. PMF has wo componen s, he p o on g adien ( ∆ pH) and he memb ane po en ial ( ∆Ψ ), and is esponsible o he ATP syn hesis by he ATP syn hase o he hylakoid memb ane, a p ocess ha is subjec ed o edox egula ion [ 46 – 48 ]. O he hylakoid-localised anspo p ocesses, such as he K + exchange an ipo e 3 (KEA3), ope a e o ha monise PMF wi h me abolic equi emen s. KEA3 ac s modula ing ATP syn hesis hence elaxing ∆ pH by p o on expo om he hylakoid lumen [ 49 ]. KEA3 ac i i y migh be con olled ia he s oma-loca ed C- e minal domain, possibly by moni o ing he NADPH/NADP + a io [ 50 ]. Wang and co-wo ke s ha e also p oposed a second ype o edox egula ion in ol ing an N- e minal Cys esidue acing he lumen side [50]. The ques ion a ising is why plan s ha e wo CEF sys ems, NDH and PGR5/PGRL1 complexes, bo h o hem ha ing a ole in p o ec ion agains ligh s ess. In chlo oplas s, mul iple in e connec ed biosyn he ic pa hways a e ope a ing a he same ime. In gen- e al, hese p ocesses a e NADPH and ATP consuming, bu he NADPH/ATP a io o suppo each me abolic pa hway is di e se and his a io mus be adap ed o speci ic needs (i.e., Cal in–Benson cycle, ni ogen and sulphu assimila ion, lipid biosyn hesis, isop enoid p ecu so biosyn hesis, e c.). Reaching a p ope balance be ween NADPH and ATP, in eg a ing ligh (ene gy inpu ), plan de elopmen and cell ca abolism migh in ol e dynamic p ocesses ac ing a he pho osyn hesis le el (Figu e 1). Acco ding o his easoning, i would be in e es ing o in es iga e and shed mo e ligh on he ole o CEF in plan physiology/me abolism unde non-s ess condi ions. 2.1. The NDH Complex The A abidopsis NDH complex is composed o 29 subuni s (11 o which a e plas id- encoded) g ouped in i e subcomplexes [ 51 ]. The chlo oplas NDH complex, which has a molecula mass o app oxima ely 700 kDa, shows homology wi h he espi a o y complex I o bac e ia and mi ochond ia. This complex is p esen as a monome ic complex associa ed wi h PSI [ 52 ]. Some au ho s ha e ecen ly de e mined ha in A. haliana plan s g own unde non-s essing condi ions he PSI:NDH a io is abou 45.4 [ 53 ]. Conce ning edox egula ion o NDH ac i i y, i was p oposed ha NTRC exe s an ac i a ing e ec , [ 54 ] whe eas TRX m4 was sugges ed o be a nega i e egula o [ 55 ] (Figu e 1). Whe eas se e al An ioxidan s 2021,10, 1789 4 o 17 NDH subuni s we e iden i ied in a co-immunop ecipi a ion assay using an i-NTRC an i- bodies, suppo ing hei edox egula ion [ 54 ], he mechanism o TRX m4-dependen NDH egula ion emains o be de e mined [ 55 ]. Since, as a as we know, no hiol/disulphide mechanisms we e p oposed o di ec ly egula e NDH ac i i y, he pos - ansla ional edox egula ion o NDH emains elusi e. Ne e heless, hough indi ec ly, edox signalling a ec s NDH egula o y p o eins ac ing a ansc ip ional o ansla ional le els. Fo in- s ance, i is known ha hyd ogen pe oxide can igge he ac i i y o he NDH complex in ba ley [ 56 ] and ha low le els o asco bic acid o educed glu a hione down egula e genes coding o NDH subuni s [ 57 ]. Pa adoxically, hough many yea s ago phospho yla ion was desc ibed o ac i a e he NDH complex [ 58 ], no di ec edox egula ion has been p o ed so a o his pho osyn he ic complex. The ques ion is whe he NDH- and PGR5/PGRL1- dependen CEF in eg a e di e en ypes o chlo oplas cues o balance he NADPH/ATP a io unde a b oad ange o en i onmen al and de elopmen al si ua ions. In e es ingly, se e al o chid species, plan s ha ha e a he e o ophic phase in hei li e cycle, ha e los he NDH complex, which led o p opose ha he loss o NDH complex migh be necessa y o hese plan s [ 59 ]. The ques ion is whe he his appa en ly TRX-independen p ocess is ela ed o he ole o NDH in non-pho osyn he ic o gans as ui s [60]. An ioxidan s 2021, 10, x FOR PEER REVIEW 4 o 18 Figu e 1. Pho osyn he ic p ocesses in ol ed in balancing he NADPH/ATP a io in A abidopsis chlo oplas s. TRXs ecei e edox equi alen s om he linea elec on low and con ol he cyclic elec on low o ine- une he p o on mo i e o ce and he ATP syn hesis. A he same ime, KEA3 modula es he ATPase ac i i y con olled by TRXs /m and NTRC. The soluble elec on ca ie s e edoxin (Fd) and plas ocyanin (PC) ope a e a bo h sides o he hylakoid memb ane connec ing PSI wi h he CEF complexes and Cy b 6 , espec i ely. G een a ows ep esen di ec ac i a ion media ed by TRXs o NTRC; unca ed ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. P o ein complexes we e schema- ised o a be e unde s anding. 2.1. The NDH Complex The A abidopsis NDH complex is composed o 29 subuni s (11 o which a e plas id- encoded) g ouped in i e subcomplexes [51]. The chlo oplas NDH complex, which has a molecula mass o app oxima ely 700 kDa, shows homology wi h he espi a o y complex I o bac e ia and mi ochond ia. This complex is p esen as a monome ic complex associ- a ed wi h PSI [52]. Some au ho s ha e ecen ly de e mined ha in A. haliana plan s g own unde non-s essing condi ions he PSI:NDH a io is abou 45.4 [53]. Conce ning edox egula ion o NDH ac i i y, i was p oposed ha NTRC exe s an ac i a ing e ec , [54] whe eas TRX m4 was sugges ed o be a nega i e egula o [55] (Figu e 1). Whe eas se e al NDH subuni s we e iden i ied in a co-immunop ecipi a ion assay using an i- NTRC an ibodies, suppo ing hei edox egula ion [54], he mechanism o TRX m4-de- penden NDH egula ion emains o be de e mined [55]. Since, as a as we know, no hiol/disulphide mechanisms we e p oposed o di ec ly egula e NDH ac i i y, he pos - ansla ional edox egula ion o NDH emains elusi e. Ne e heless, hough indi ec ly, edox signalling a ec s NDH egula o y p o eins ac ing a ansc ip ional o ansla ional le els. Fo ins ance, i is known ha hyd ogen pe oxide can igge he ac i i y o he NDH complex in ba ley [56] and ha low le els o asco bic acid o educed glu a hione down- egula e genes coding o NDH subuni s [57]. Pa adoxically, hough many yea s ago phospho yla ion was desc ibed o ac i a e he NDH complex [58], no di ec edox egu- la ion has been p o ed so a o his pho osyn he ic complex. The ques ion is whe he NDH- and PGR5/PGRL1-dependen CEF in eg a e di e en ypes o chlo oplas cues o balance he NADPH/ATP a io unde a b oad ange o en i onmen al and de elopmen al si ua ions. In e es ingly, se e al o chid species, plan s ha ha e a he e o ophic phase in Figu e 1. Pho osyn he ic p ocesses in ol ed in balancing he NADPH/ATP a io in A abidopsis chlo oplas s. TRXs ecei e edox equi alen s om he linea elec on low and con ol he cyclic elec on low o ine- une he p o on mo i e o ce and he ATP syn hesis. A he same ime, KEA3 modula es he ATPase ac i i y con olled by TRXs /m and NTRC. The soluble elec on ca ie s e edoxin (Fd) and plas ocyanin (PC) ope a e a bo h sides o he hylakoid memb ane connec ing PSI wi h he CEF complexes and Cy b 6 , espec i ely. G een a ows ep esen di ec ac i a ion media ed by TRXs o NTRC; unca ed ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. P o ein complexes we e schema ised o a be e unde s anding. An ioxidan s 2021,10, 1789 5 o 17 2.2. The PGR5/PGRL1 Complex The PGR5/PGRL1 complex is o med by wo subuni s and exe s a pho o-p o ec i e ole agains high-ligh media ed s ess (Figu e 1) [ 61 , 62 ]. Unlike NDH, he e a e solid expe imen al da a showing he edox- egula ion o PGR5 [ 55 , 63 , 64 ]. In line wi h his no ion, i was epo ed ha TRXs mcollec i ely down- egula e he PGR5/PGRL1 complex [ 63 ]. In plan a, TRX m4 down egula es PGR5 ac i i y by educing PGRL1 (Figu e 1) [ 55 ]. In addi ion, he ele ance o he egula ion o PGR5/PGRL1 on he chlo oplas edox s a e was e idenced by he eco e y o enzyme educ ion in he n c pg 5 A abidopsis double mu an [65]. The cyanobac e ia Synechocys is sp. con ains PGR5 bu no PGRL1 [ 66 ]. Ne e heless, in spi e o he low simila i y be ween he cyanobac e ial p o ein SII1217 and PGRL1, bo h p o eins migh be unc ionally ela ed, sugges ing a pu a i e p oka yo ic o igin o PGRL1. In e es ingly, A abidopsis PGRL1 has six cys eine esidues whe eas cyanobac e ial SII1217, which has no been shown o be edox- egula ed, has only h ee [ 63 , 64 ]. Anyway, Synechocys is media es he non-pho ochemical educ ion o PQ possibly ia CEF h ough he NDH-1 complex [ 67 , 68 ]. Ano he aqua ic o ganism, he ma ine angiospe m Zos e a ma ina, conse es he wo CEF sys ems and sha es wi h land plan s a simila esponse o espond o excess adia ion [69]. 2.3. Fe edoxins: Ac i e Playe s Balancing Linea and Cyclic Elec on Flows? Chlo oplas Fds a e small p o eins con aining a [2Fe:2S] clus e wi h low edox po- en ials. These p o eins egula e elec on pa i ioning in plan chlo oplas s by ans e - ing elec ons om pho o- educed PSI o di e en s omal p o eins such as Fd NADP + educ ase (FNR) o FTR, as well as o he hylakoid-loca ed CEF sys ems NDH and PGR5/PGRL1 [ 70 ]. A abidopsis ha bou s ou chlo oplas ic Fd iso o ms, namely FD1 (AT1G10960), FD2 (AT1G60950), FDC1 (AT4G14890) and FDC2 (AT1G32550) [ 71 , 72 ]. FD1 and FD2 accoun o 7% and 90% o he o al lea Fd, espec i ely [ 73 ]. The p esence o se e al Fd iso o ms in plan s sugges s he exis ence o speci ic a ge s o hese enzymes. In his ega d, i was hypo hesised ha FD1 would con ibu e o CEF and FD2 o LEF [ 74 – 77 ]. FDC1 and FDC2 ha e an addi ional ex ension a he C- e minus, nea hei ac i e si es, as well as highe edox po en ials han FD2, hence FDC1 and FDC2 can be conside ed a ypical Fds [ 71 , 72 ]. Unlike FD1 and FD2, FDC1 is no able o in e ac wi h FNR; ne e heless, i can in e ac wi h he CEF complexes NDH and PGR5/PGRL1 o wi h FTR [ 72 ]. These esul s sugges a ole o FDC1 in pa i ioning p o iding elec ons o speci ic chlo oplas p ocesses. Al hough he e is no expe imen al e idence so a , he possibili y canno be disca ded ha FDC2 migh ha e a simila unc ion o FDC1. I s unc ional signi icance in plan s was p o en in ice, whe e a mu a ion in he FDC2 o holog HDY1 p o okes lea yellowing and a delay in lowe ing ime [78]. In pho osyn he ic o ganisms, he docking si e a PSI, o med by he subuni s PsaD and PsaE, allows he elec onic ans e be ween Fds and PsaC [ 79 ]. Rema kably, A abidopsis has wo iso o ms o PsaD and PsaE [ 72 ], hus, i is emp ing o specula e ha he combina ion o hese iso o ms migh cons i u e auxilia y docking si es o chlo oplas Fds. I his we e he case, he dono si e o PSI would also play an ac i e ole in pho osyn hesis elec on pa i ioning and edox egula ion. 3. Redox Regula ion o Non-Pho ochemical Quenching Ligh ene gy eaching he chlo oplas can be ei he emi ed as chlo ophyll luo es- cence o quenched by pho ochemical (qP) and non-pho ochemical mechanisms (qN o NPQ). When qP is no su icien o assimila e all he abso bed ene gy, a ac ion o i mus be eleased as hea by NPQ. NPQ has di e en componen s: qE (ene gy-dependen quenching), qZ (zeaxan hin-dependen quenching), qT (s a e- ansi ion quenching), qI (pho o-inhibi o y quenching) and qH (sus ained and slowly e e sible quenching) [ 80 – 82 ]. Behind all hese pho op o ec i e mechanisms, he e is a dynamic edox ne wo k in which An ioxidan s 2021,10, 1789 6 o 17 TRXs play ac i e oles [ 28 ]. I ollows now a discussion o he ele ance o TRXs in he egula ion o he di e en NPQ componen s (Figu e 2). An ioxidan s 2021, 10, x FOR PEER REVIEW 6 o 18 NPQ). When qP is no su icien o assimila e all he abso bed ene gy, a ac ion o i mus be eleased as hea by NPQ. NPQ has di e en componen s: qE (ene gy-dependen quenching), qZ (zeaxan hin-dependen quenching), qT (s a e- ansi ion quenching), qI (pho o-inhibi o y quenching) and qH (sus ained and slowly e e sible quenching) [80– 82]. Behind all hese pho op o ec i e mechanisms, he e is a dynamic edox ne wo k in which TRXs play ac i e oles [28]. I ollows now a discussion o he ele ance o TRXs in he egula ion o he di e en NPQ componen s (Figu e 2). Figu e 2. Schema ic ep esen a ion o he edox egula ion media ed by TRXs and m o he NPQ componen s in A abidop- sis. The ype o in e ac ion is ei he ep esen ed in g een ( edox ype) o in ed (non- edox ype). A ows ep esen ac i a- ion; unca ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. De ec s in NDH can a ec ∆pH o ma ion and lead o impai ed ac i a ion o NPQ ene gy-dependen quenching [83]. The pigmen zeaxan hin is ano he key componen o NPQ in plan s, being esponsible o pH-independen qZ, and ene gy-dependen quench- ing (qE). In excess ligh , he high pH g adien a ou s p o ona ion o PsbS subuni o PSII, igge ing qE and ac i a ing he enzyme iolaxan hin de-epoxidase (VDE), which ca aly- ses he con e sion o iolaxan hin o zeaxan hin in he hylakoid lumen. This enzyme is s imula ed by he hylakoid lumen acidi ica ion upon illumina ion and is ac i e in i s ox- idised s a e [84,85]. As TRXs m deli e elec ons in o he hylakoid lumen h ough CCDA and HCF164 [19,44], hese TRXs can indi ec ly egula e enzymes such as VDE (Figu e 2). VDE was iden i ied as a pu a i e a ge o a lumenal disulphide- o ming enzyme e med Lumen Thiol Oxido educ ase1 (LTO1), sugges ing ha i could play a key ole in he e- dox-dependen egula ion o zeaxan hin le els [86]. The o he enzyme pa icipa ing in he xan hophyll cycle, zeaxan hin epoxidase (ZE), which ca alyses he con e sion o zeaxan- hin and an he axan hin o egene a e iolaxan hin, is also egula ed by TRXs. Mu an plan s lacking TRXs m accumula e highe le els o agg ega ed/inac i a ed ZE and zeaxan- hin [87]. In addi ion, NTRC de icien plan s showed inc eased zeaxan hin le els and ele- a ed qE; howe e , hough NTRC can educe ZE agg ega es in i o, no al e a ion o ZE edox s a e was obse ed in n c mu an plan s. Ra he , he inc eased ∆pH unde low and mode a e ligh in ensi ies in n c plan s seems o be esponsible o he ac i a ion o VDE [88]. 3.1. Pho o-P o ec i e Quenching in LHCII: Is Lipocalin Subjec ed o Redox Regula ion? A new componen o pH-independen NPQ, sus ained quenching o qH, ha p e- cedes PSII damage and epai , was ecen ly iden i ied in a sea ch o supp esso s o npq4 Figu e 2. Schema ic ep esen a ion o he edox egula ion media ed by TRXs and mo he NPQ componen s in A abidopsis. The ype o in e ac ion is ei he ep esen ed in g een ( edox ype) o in ed (non- edox ype). A ows ep esen ac i a ion; unca ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. De ec s in NDH can a ec ∆ pH o ma ion and lead o impai ed ac i a ion o NPQ ene gy-dependen quenching [ 83 ]. The pigmen zeaxan hin is ano he key componen o NPQ in plan s, being esponsible o pH-independen qZ, and ene gy-dependen quenching (qE). In excess ligh , he high pH g adien a ou s p o ona ion o PsbS subuni o PSII, igge ing qE and ac i a ing he enzyme iolaxan hin de-epoxidase (VDE), which ca alyses he con e sion o iolaxan hin o zeaxan hin in he hylakoid lumen. This enzyme is s imula ed by he hylakoid lumen acidi ica ion upon illumina ion and is ac i e in i s oxidised s a e [ 84 , 85 ]. As TRXs mdeli e elec ons in o he hylakoid lumen h ough CCDA and HCF164 [ 19 , 44 ], hese TRXs can indi ec ly egula e enzymes such as VDE (Figu e 2). VDE was iden i ied as a pu a i e a ge o a lumenal disulphide- o ming enzyme e med Lumen Thiol Oxido educ ase1 (LTO1), sugges ing ha i could play a key ole in he edox- dependen egula ion o zeaxan hin le els [ 86 ]. The o he enzyme pa icipa ing in he xan hophyll cycle, zeaxan hin epoxidase (ZE), which ca alyses he con e sion o zeaxan hin and an he axan hin o egene a e iolaxan hin, is also egula ed by TRXs. Mu an plan s lacking TRXs maccumula e highe le els o agg ega ed/inac i a ed ZE and zeaxan hin [ 87 ]. In addi ion, NTRC de icien plan s showed inc eased zeaxan hin le els and ele a ed qE; howe e , hough NTRC can educe ZE agg ega es in i o , no al e a ion o ZE edox s a e was obse ed in n c mu an plan s. Ra he , he inc eased ∆ pH unde low and mode a e ligh in ensi ies in n c plan s seems o be esponsible o he ac i a ion o VDE [88]. 3.1. Pho o-P o ec i e Quenching in LHCII: Is Lipocalin Subjec ed o Redox Regula ion? A new componen o pH-independen NPQ, sus ained quenching o qH, ha p ecedes PSII damage and epai , was ecen ly iden i ied in a sea ch o supp esso s o npq4 mu an plan s lacking PsbS [ 82 , 89 ] (Figu e 3). This ∆ pH-independen mechanism, simila o ha in e e g eens, is dependen on a plas id lipocalin (LCNP), localised in he lumen, and ela ed An ioxidan s 2021,10, 1789 7 o 17 o he appea ance o new quenching si es in LHCII. LCNP is nega i ely egula ed by SOQ1 (Supp esso o quenching 1), a TRX-like/ β -p opelle p o ein, h ough a mechanism ha is so a unknown [ 82 ]. Since Cys esidues o he TRX-like lumenal ac i e-si e mo i o SOQ1 a e equi ed o he supp ession o qH, and LCNP con ains six conse ed Cys, a pu a i e edox-dependen egula ion o LCNP by SOQ1 was sugges ed. Howe e , he down- egula ion o SOQ1 unde d ough s ess and he inabili y o e e se he elec opho e ic mobili y o LCNP wi h DTT in soq1 mu an s, a gues agains i , sugges ing a he an inc eased ac i i y o LCNP due o he dec ease in SOQ1 le els unde s ess condi ions [ 82 ]. Ne e heless, he inding o SOQ1 as a possible NTRC in e ac o [ 54 ] and he ecen iden i ica ion o LTO1, in a gene ic sc een o supp esso s o soq1 npq4 by B u and co- wo ke s (2020), has aised again he ques ion o a possible edox egula ion o LCNP [ 90 ]. The pa icipa ion o NTRC in he down- egula ion o qH has ecen ly been p oposed [91]. An ioxidan s 2021, 10, x FOR PEER REVIEW 7 o 18 mu an plan s lacking PsbS [82,89] (Figu e 3). This ∆pH-independen mechanism, simila o ha in e e g eens, is dependen on a plas id lipocalin (LCNP), localised in he lumen, and ela ed o he appea ance o new quenching si es in LHCII. LCNP is nega i ely egu- la ed by SOQ1 (Supp esso o quenching 1), a TRX-like/β-p opelle p o ein, h ough a mechanism ha is so a unknown [82]. Since Cys esidues o he TRX-like lumenal ac i e- si e mo i o SOQ1 a e equi ed o he supp ession o qH, and LCNP con ains six con- se ed Cys, a pu a i e edox-dependen egula ion o LCNP by SOQ1 was sugges ed. Howe e , he down- egula ion o SOQ1 unde d ough s ess and he inabili y o e e se he elec opho e ic mobili y o LCNP wi h DTT in soq1 mu an s, a gues agains i , sug- ges ing a he an inc eased ac i i y o LCNP due o he dec ease in SOQ1 le els unde s ess condi ions [82]. Ne e heless, he inding o SOQ1 as a possible NTRC in e ac o [54] and he ecen iden i ica ion o LTO1, in a gene ic sc een o supp esso s o soq1 npq4 by B u and co-wo ke s (2020), has aised again he ques ion o a possible edox egula ion o LCNP [90]. The pa icipa ion o NTRC in he down- egula ion o qH has ecen ly been p oposed [91]. Figu e 3. Regula ion o he NPQ componen s in A abidopsis chlo oplas s. TRXs m a e key edox playe s in he egula ion o NPQ in plan s as hey ans e educing equi alen s in o he hylakoid lumen h ough he p o eins CCDA and HFC164. The hylakoid p o ein LTO1, wi h an oxidan ole, con ibu es o main aining he edox homeos asis in he chlo oplas lumen. G een a ows ep esen ac i a ion media ed by TRXs o NTRC; unca ed ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. P o ein complexes we e schema ised o a be e unde s anding. Recen ly, a new playe in qH egula ion p esen in all plas id-con aining o ganisms, ROQH1 (RELAXATION OF QH1), wi h an an agonis ic unc ion o LCNP, was iden i ied. ROQH1 is a s oma lamella memb ane-associa ed p o ein, belonging o a NAD(P)H-de- penden a ypical sho -chain dehyd ogenase/ educ ase (SDR) sub amily, ha p oduces a dose-dependen elaxa ion o qH, u ning he LCNP c ea ed quenching si es back in o ligh -ha es ing si es [92]. While SOQ1 is p esen in Chlamydomonas and Synechocys is sp. as wo independen p o eins co esponding o he HAD and he NHL/TRX-like domain o SOQ1, and ROQH1 homologues we e iden i ied in Synechocys is sp. PCC 6803, he low sequence conse a ion be ween LCNP homologues makes i di icul o analyse whe he qH is a conse ed mech- anism om cyanobac e ia. Figu e 3. Regula ion o he NPQ componen s in A abidopsis chlo oplas s. TRXs ma e key edox playe s in he egula ion o NPQ in plan s as hey ans e educing equi alen s in o he hylakoid lumen h ough he p o eins CCDA and HFC164. The hylakoid p o ein LTO1, wi h an oxidan ole, con ibu es o main aining he edox homeos asis in he chlo oplas lumen. G een a ows ep esen ac i a ion media ed by TRXs o NTRC; unca ed ed lines, inhibi ion. A dashed line indica es a hypo he ical in e ac ion. P o ein complexes we e schema ised o a be e unde s anding. Recen ly, a new playe in qH egula ion p esen in all plas id-con aining o ganisms, ROQH1 (RELAXATION OF QH1), wi h an an agonis ic unc ion o LCNP, was iden i ied. ROQH1 is a s oma lamella memb ane-associa ed p o ein, belonging o a NAD(P)H- dependen a ypical sho -chain dehyd ogenase/ educ ase (SDR) sub amily, ha p oduces a dose-dependen elaxa ion o qH, u ning he LCNP c ea ed quenching si es back in o ligh -ha es ing si es [92]. While SOQ1 is p esen in Chlamydomonas and Synechocys is sp. as wo independen p o eins co esponding o he HAD and he NHL/TRX-like domain o SOQ1, and ROQH1 homologues we e iden i ied in Synechocys is sp. PCC 6803, he low sequence conse a ion be ween LCNP homologues makes i di icul o analyse whe he qH is a conse ed mechanism om cyanobac e ia. An ioxidan s 2021,10, 1789 8 o 17 3.2. Redis ibu ion o Exci a ion Ene gy be ween he PSs: Role o Redox Regula ion o LHCII Kinase and Cy b6 Assembly in S a e T ansi ions Ligh quali y in he na u al en i onmen is a iable, hus chlo oplas s equi e a dy- namic sys em allowing he dis ibu ion o exci a ion ene gy be ween he wo pho osys ems, p e en ing imbalance in PETC in pho osyn he ic o ganisms, and a oiding pho oinhibi ion especially unde luc ua ing ligh condi ions. In plan s and algae, he e-dis ibu ion o exci a ion ene gy is dependen on s a e ansi ions media ed by he phospho yla ion o he ligh -ha es ing complex II (LHCII) by a se ine/ h eonine LHCII kinase, known as S 7 o S n7 in Chamydomonas einha d ii and A. haliana, espec i ely. The egula ion o LHCII phospho yla ion and i s e ec on he mig a ion o LHCII om PSII o he PSI is known o many yea s: LHCII kinase is ac i a ed by educed PQ in low ligh and inac i a ed by TRX in high ligh [ 93 ]. Mo e ecen ly, a ele an ole o he Rieske i on-sulphu p o ein o he Cy b 6 complex was p oposed, in which he mo emen o he p o ein wi hin his complex, a e binding o educed PQ, gene a es a con o ma ional change in he complex ha in u ns ac i a es LHCII kinase [ 94 ]. The physical in e ac ion o S 7 wi h he Cy b 6 complex and PSI was demons a ed by co-immunop ecipi a ion expe imen s in Chlamydomonas and he Rieske p o ein was iden i ied as he in e ac o wi h S 7 [95]. The opology o S 7 was analysed using a agged p o ein, e ealing ha he p o ein con ains a ansmemb ane domain, wi h he kinase ac i i y a he s omal side and he N- e minal egion, con aining he wo conse ed Cys wi hin algae and plan LCHII kinases, in he lumen. The disul ide bond be ween hese Cys is essen ial o he phospho yla ion o LHCII, sugges ing ha edox egula ion migh be c i ical o S 7 ac i i y [ 95 ]. This egula ion could be media ed by luminal TRX-like p o eins, such as HCF164 and CCDA, which we e p oposed o pa icipa e in he ansduc ion o TRX signals om he s oma [ 42 , 96 ]. The wo k o Shapiguzo e al. (2016) e ealed, howe e , ha he disul ide b idge in bo h Ss 7 and S n7 is main ained du ing ac i a ion and inac i a ion o he kinases, which ques ions he edox egula ion o LHCII kinase [ 97 ]. I was sugges ed ha wo conse ed Cys esidues o LHCII kinase loca ed in he s oma, bu no conse ed in algae, could be egula ed by he FTR/TRX sys em, howe e , he analysis o he speci ici y o TRXs and min he p ocess has gi en con adic o y esul s. While in i o analysis showed di ec in e ac ion be ween TRX and S n7 [ 98 ] and an inhibi o y e ec o bo h TRX and mon LHCII phospho yla ion was shown [ 99 ], he analysis o xm1m2 mu an s unde luc ua ing ligh condi ions no only sugges ed he ac i a ion o S n7 as a compensa o y mechanism o inc ease pho osyn hesis du ing low ligh pe iods, bu also he essen iali y o his egula ion o comple e ac i a ion o pho osyn hesis du ing high ligh pe iods [ 100 ]. Mo e ecen ly, s udies pe o med wi h obacco plan s ha e e ealed ha plan s o e -exp essing TRX m, bu no TRX , showed a loss o LHCII phospho yla ion unde low ligh , sugges ing a ole o TRX min he deac i a ion o S n7. Mo eo e , since he pheno ype o TRX m o e -exp essing plan s mimics ha o wild- ype plan s unde high ligh , when LHCII is no phospho yla ed, he esul s sugges a ole o TRX min he deac i a ion o S n7 unde high ligh [ 101 ]. Recen ly, i was epo ed ha he al e ed chlo oplas hiol edox s a e in n c mu an s and NTRC o e -exp essing plan s p o okes a e-dis ibu ion o exci a ion ene gy be ween he wo PSs, al e ing s a e ansi ions, h ough a mechanism ha is p obably independen o S n7 bu a he media ed by CP29.3, a monome ic LHC p o ein wi h a conse ed Cys esidue [ 91 ]. The p ecise ole o edox egula ion on he deac i a ion o LHCII kinase and he conse a ion o his mechanism o egula ion in bo h plan a and algae emains o be de e mined. I is wo h men ioning ha he impo ance o S n7 in s a e ansi ions in lowe ing plan s is no clea since loss-o - unc ion o his p o ein does no esul in signi ican al e - a ions o plan de elopmen . Ins ead, only when he s n7 mu a ion is combined wi h mu a- ions leading o a dec eased pool o PQ he g ow h a e and s a e ansi ions a e a ec ed, showing ha hese ansi ions a e c i ical when linea elec on low is al e ed [ 102 , 103 ]. The change in he edox s a us o he PQ pool p o okes long- e m changes in gene exp ession o Lhcb1, p obably adjus ing he an enna size as an addi ional mechanism o balance he An ioxidan s 2021,10, 1789 9 o 17 use o exci a ion ene gy be ween he wo PSs [ 104 ]. The egula ion o S n7 by he PQ edox s a e [102] suppo s his hypo hesis. Rema kably, he pa icipa ion o HCF164 in Cy b 6 assembly was also p oposed [ 42 ]. Apo-cy and he haem g oups a e bo h syn hesised a he s omal side o he hylakoid memb ane and a e anspo ed independen ly o he lumen. Once in he lumen, he educed haem g oup is a ached o he binding si e o Cy by means o a hioe he bond. Fo his, he apo-cy mus be main ained in a educed s a e. The ans e o elec ons om he s oma o he lumen and he p ese a ion o apo-cy in a educed s a e is ca ied ou ia CCDA and HCF164, as sugges ed by he analysis o A abidopsis ccdA and hc 164 mu an s, which show de ec i e Cy b 6 accumula ion [ 42 , 43 ]. In C. einha d ii CCS5, and p obably CCS4, homologues o HCF164, could educe he haem binding si e in apo-cy [ 96 ]. Recen s udies poin ed ou he ole o TRXs min he ans e o elec ons, needed o Cy educ ion, om he s oma o he lumen h ough HCF164 [19,96]. Finally, he o ma ion o he i on-sulphu clus e in he Rieske p o ein, PSI and Fd, depends on he ac i i y o wo class- wo GRXs, ha a e unable o educe disulphide b idges. In chlo oplas s, simila ly o bac e ia, dime s o GRX14 and GRX16, oge he wi h he sca old p o eins BOL1 and BOL4, can bind 2Fe:2S clus e s and consequen ly ans e hem o Fd in i o [105,106]. 3.3. Pho odamage and Repai o PSII: Redox Regula ion o D1 Deg ada ion and PsbO S abili y PSII is highly suscep ible o excess ligh , which leads o i s i e e sible damage, p o oking deg ada ion o i s co e p o eins, such as D1. D1 is apidly eplaced in he PSII epai cycle so ha pho oinhibi ion only occu s when he a e o epai is slowe han he a e o damage [ 107 ]. In con as , he eco e y o pho o-inhibi ed PSI occu s e y slowly. Fo his eason, PSI is p o ec ed om pho oinhibi ion by se e al mechanisms, which include a dec eased a e o elec on ans e o PSI due o PSII deg ada ion and down- egula ion o elec on anspo h ough Cy b 6 , p obably media ed by PGR5/PGRL1 [ 62 ]. The ele ance o he la e in he p o ec ion o PSI om pho oinhibi ion is e ealed by he esul s by Lima-Melo and co-wo ke s (2018), showing ha pg 5 mu an plan s con ained dec eased le els o PsaB co e subuni and se e ely dec eased Fd educ ion unde high ligh condi ions. The eco e y o PSI in hese plan s seems o be dependen on he eo ganisa ion o he ligh -ha es ing an enna, h ough inc eased phospho yla ion o LHCII. In addi ion, a “ ese e” PSI* complex, lacking LHCI an ennae and pe iphe al subuni s, could help o suppo PETC unde PSI pho oinhibi ion [108]. PSII consis s o mo e han 30 in eg al memb ane p o eins, including he ca aly ic eac ion cen e and he chlo ophyll-binding p o eins, s abilised by ex insic p o eins loca ed a he lumenal side ha o m pa o he Oxygen E ol ing Complex (OEC). This complex is o med by ou ex insic p o eins, PsbO, PsbP, PsbQ and PsbR. PsbO in e ac s wi h se e al co e subuni s o PSII and seems o p o ide a basal s uc u e o which he o he OEC subuni s a e bound [109]. The damage o p o eins in he eac ion cen es o he PSII and hei epai cons i u e he pho o-inhibi o y quenching, qI, componen o NPQ (Figu es 2and 3). Damaged D1, and in some cases D2, CP43 and PsbH o he PSII co e, a e subjec ed o Deg-dependen p o eolysis unde condi ions o PSII pho o-damage, by Deg7, which is associa ed wi h he s omal side o he hylakoid memb anes. In addi ion, a ole o s omal and lumenal Deg p o eases in he deg ada ion o PSII co e p o eins was sugges ed [ 107 , 110 ]. Since damaged D1 p o ein is associa ed wi h lowe pho osyn he ic ac i i y, a mechanism o he deg ada ion o he damaged p o ein is essen ial o main ain pho osyn he ic pe o mance. Howe e , he damage o he Mn-clus e seems o be a p ima y s ep leading o D1 deg ada ion media ed by he ac i i y o hese p o eases [ 111 , 112 ]. As a i s s ep o he epai o PSII and he deg ada ion o speci ic co e p o eins, he PSII dime s o supe complexes, loca ed o he g ana egions o he hylakoid, mus disagg ega e o monome s and mig a e o s omal hylakoids [ 113 ]. 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