**Author details**

Jean-David Rochaix\*

Address all correspondence to: Jean-David.Rochaix@unige.ch

Departments of Molecular Biology and Plant Biology, University of Geneva University,

Geneva, Switzerland

## **References**

isoprenoids as well as plastid protein synthesis, the redox state of the photosynthetic electron transport chain and ROS generated under specific stress conditions. Moreover, a complex signaling network is operating within chloroplasts comprising several protein kinases and phosphatases, ion channels, and specific metabolites which act as signals and for the commu‐ nication between chloroplast and nucleus. However, the signaling chains connecting these different components are still largely unknown and their identification remains an important

The flexibility of the thylakoid membrane is truly remarkable. Although it is crowded with proteins, it still allows for efficient remodeling of the photosynthetic complexes within the thylakoid membrane especially in response to changes in the quality and quantity of light. Among these responses, state transitions and NPQ have been studied extensively and some of the underlying molecular mechanisms have been elucidated. However, many questions remain open. We still do not fully understand how the Stt7/STN7 kinase that plays a central role in state transitions and chloroplast signaling is activated and inactivated as a result of perturbations of the chloroplast redox poise. From an evolutionary point of view, it is partic‐ ularly interesting to compare these adaptive responses in different photosynthetic organisms such as plants, fresh water and marine algae and cyanobacteria. In this respect, NPQ, the dissipation of excess excitation energy as heat in the light-harvesting systems of the photo‐ systems, is of great importance and it is widely used in the plant kingdom. Recent studies on NPQ in different photosynthetic organisms raise several questions regarding the evolution of this essential photoprotective mechanism. For example, it is not clear why the Lhcsr proteins were lost during the transition from aquatic to land plants. Moreover, the qE process in most algae derived by secondary endosymbiosis from a red algal ancestor differs from that in extant red algae. All of these derived algae possess a xanthophyll cycle and Lhcsr-related proteins which are apparently absent in red algae [87] and which have been suggested to be derived from green algae [143,144]. It will clearly be important and challenging to elucidate these

I thank Nicolas Roggli for preparing the figures and Michel Goldschmidt-Clermont for critical reading of the manuscript. Work in the author's laboratory was supported by grants from the

challenge for future research.

40 Applied Photosynthesis - New Progress

evolutionary puzzles.

**Acknowledgment**

**Author details**

Jean-David Rochaix\*

Swiss National Science Foundation.

Address all correspondence to: Jean-David.Rochaix@unige.ch


[26] Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D. Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol. 2010;8(1):e1000288.

[12] Minagawa J, Takahashi Y. Structure, function and assembly of Photosystem II and its

[13] Drop B, Webber-Birungi M, Yadav SK, Filipowicz-Szymanska A, Fusetti F, Boekema EJ, et al. Light-harvesting complex II (LHCII) and its supramolecular organization in

[14] Nield J, Kruse O, Ruprecht J, da Fonseca P, Buchel C, Barber J. Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus photosystem II complexes allows for comparison of their oxygen-evolving complex organization. J

[15] Tokutsu R, Kato N, Bui KH, Ishikawa T, Minagawa J. Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii. J Biol Chem.

[16] Gunning BES, Schwartz OM. Confocal microscopy of thylakoid autofluorescence in relation to origin of grana and phylogeny in the green algae. Aust J Plant Physiol

[17] Lemeille S, Rochaix JD. State transitions at the crossroad of thylakoid signalling

[18] Wollman FA. State transitions reveal the dynamics and flexibility of the photosynthetic

[19] Niyogi KK. PHOTOPROTECTION REVISITED: Genetic and Molecular Approaches.

[20] Niyogi KK, Truong TB. Evolution of flexible non-photochemical quenching mecha‐ nisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol.

[21] Vener AV, van Kan PJ, Rich PR, Ohad II, Andersson B. Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-

[22] Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA. The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. Embo J.

[23] Depège N, Bellafiore S, Rochaix JD. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science. 2003;299:1572–1575.

[24] Bellafiore S, Barneche F, Peltier G, Rochaix JD. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature. 2005;433:892–895.

[25] Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, Rochaix JD. Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol. 2009;7(3):e45.

Chlamydomonas reinhardtii. Biochim Biophys Acta. 2014;1837(1):63–72.

light-harvesting proteins. Photosynth Res. 2004;82(3):241–263.

Biol Chem. 2000;275(36):27940–27946.

pathways. Photosynth Res. 2010;106:33-46.

apparatus. Embo J. 2001;20(14):3623–3630.

Annu Rev Plant Physiol Plant Mol Biol. 1999;50:333–359.

turnover flash. Proc Natl Acad Sci U S A. 1997;94(4):1585–1590.

2012;287(37):31574–31581.

1999;26:695–708.

42 Applied Photosynthesis - New Progress

2013;16(3):307–314.

1999;18(11):2961–2969.


irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem. 1997;272(48):30476–30482.


[51] Khorobrykh SA, Karonen M, Tyystjarvi E. Experimental evidence suggesting that H2O2 is produced within the thylakoid membrane in a reaction between plastoquinol and singlet oxygen. FEBS Lett. 2015;589(6):779–786.

irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem. 1997;272(48):30476–30482.

[39] Page ML, Hamel PP, Gabilly ST, Zegzouti H, Perea JV, Alonso JM, et al. A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J Biol Chem. 2004;279(31):32474–

[40] Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K. HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f

[41] Karamoko M, Cline S, Redding K, Ruiz N, Hamel PP. Lumen Thiol Oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in

[42] Du JJ, Zhan CY, LuY, Cui HR, Wang XY. The conservative cysteines in transmembrane domain of AtVKOR/LTO1 are critical for photosynthetic growth and photosystem II

[43] Darrouzet E, Moser CC, Dutton PL, Daldal F. Large scale domain movement in cytochrome bc(1): a new device for electron transfer in proteins. Trends Biochem Sci.

[44] Shapiguzov, A, Chai X, Fucile G, Longoni P, Zhang L, Rochaix JD. Activation of the Stt7/STN7 kinase through dynamic interactions with the cytochrome *b*6*f* complex. Plant

[45] Breyton C. Conformational changes in the cytochrome b6f complex induced by

[46] BultéL, Gans P, Rebeille F, Wollman FA. ATP control on state transitions in Chlamy‐

[47] Wunder T, Liu Q, Aseeva E, Bonardi V, Leister D, Pribil M. Control of STN7 transcript abundance and transient STN7 dimerisation are involved in the regulation of STN7

[48] Stroebel D, Choquet Y, Popot JL, Picot D. An atypical haem in the cytochrome b(6)f

[49] Kurisu G, Zhang H, Smith JL, Cramer WA. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science. 2003;302(5647):1009–1014. Epub

[50] de Lacroix de Lavalette A, Finazzi G, Zito F. b6f-Associated chlorophyll: structural and dynamic contribution to the different cytochrome functions. Biochemistry.

complex in Arabidopsis. Plant Cell. 2001;13(11):2539–2551.

activity in Arabidopsis. Frontiers in plant science. 2015;6:238.

Physiol. 2016; Mar 3. pii: pp.01893.2015. [Epub ahead of print]

inhibitor binding. J Biol Chem. 2000;275(18):13195–13201.

domonas. Biochim Biophys Acta. 1990;1020:72–80.

activity. Planta. 2013;237(2):541–558.

complex. Nature. 2003;426(6965):413–418.

Arabidopsis. Plant Cell. 2011;23(12):4462–4475.

32482. Epub 2004 May 24.

44 Applied Photosynthesis - New Progress

2001;26(7):445–451.

2003 Oct 2.

2008;47:5259–5265.


[77] Bonente G, Ballottari M, Truong TB, Morosinotto T, Ahn TK, Fleming GR, et al. Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydo‐ monas reinhardtii. PLoS Biol. 2011;9(1):e1000577.

[65] Phillip D, Ruban AV, Horton P, Asato A, Young AJ. Quenching of chlorophyll fluo‐ rescence in the major light-harvesting complex of photosystem II: a systematic study of the effect of carotenoid structure. Proc Natl Acad Sci U S A. 1996;93(4):1492–1497.

[66] Wentworth M, Ruban AV, Horton P. Kinetic analysis of nonphotochemical quenching of chlorophyll fluorescence. 2. Isolated light-harvesting complexes. Biochemistry.

[67] Holwarth AR, Miloslavina Y, Nilkens M, Jahns P. Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studies by time-resolved

[68] Kruger TP, Ilioaia C, Johnson MP, Ruban AV, Papagiannakis E, Horton P, et al. Controlled disorder in plant light-harvesting complex II explains its photoprotective

[69] Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, et al. A pigmentbinding protein essential for regulation of photosynthetic light harvesting. Nature.

[70] Fan M, Li M, Liu Z, Cao P, Pan X, Zhang H, et al. Crystal structures of the PsbS protein essential for photoprotection in plants. Nat Struct Mol Biol. 2015;22(9):729–735. [71] Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, et al. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS

[72] Betterle N, Ballottari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall'osto L, et al. Lightinduced dissociation of an antenna hetero-oligomer is needed for non-photochemical

[73] Goral TK, Johnson MP, Duffy CD, Brain AP, Ruban AV, Mullineaux CW. Lightharvesting antenna composition controls the macrostructure and dynamics of thyla‐

[74] Teardo E, de Laureto PP, Bergantino E, Dalla Vecchia F, Rigoni F, Szabo I, et al. Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids.

[75] Bergantino E, Segalla A, Brunetta A, Teardo E, Rigoni F, Giacometti GM, et al. Lightand pH-dependent structural changes in the PsbS subunit of photosystem II. Proc Natl

[76] Johnson MP, Ruban AV. Restoration of rapidly reversible photoprotective energy dissipation in the absence of PsbS protein by enhanced Deltap H. J Biol Chem.

2001;40(33):9902–9908.

46 Applied Photosynthesis - New Progress

2000;403(6768):391–395.

fluorescence. Chem Phys Lett. 2009;483:262–267.

protein. J Biol Chem. 2004;279(22):22866–22874.

Biochim Biophys Acta. 2007;1767(6):703–711.

Acad Sci U S A. 2003;100(25):15265–15270.

2011;286(22):19973–19981.

quenching induction. J Biol Chem. 2009;284(22):15255–15266.

koid membranes in Arabidopsis. Plant J. 2012;69(2):289–301.

role. Biophys J. 2012;102(11):2669–2676.


[103] Moseley J, Quinn J, Eriksson M, Merchant S. The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii. EMBO J. 2000;19(10):2139–2151.

[90] Bailleul B, Berne N, Murik O, Petroutsos D, Prihoda J, Tanaka A, et al. Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms.

[91] Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J. Recent advances in understanding

[92] Aro EM, Virgin I, Andersson B. Photoinhibition of photosystem II. Inactivation, protein

[93] Puthiyaveetil S, Tsabari O, Lowry T, Lenhert S, Lewis RR, Reich Z, et al. Compartmen‐ talization of the protein repair machinery in photosynthetic membranes. Proc Natl

[94] Vainonen JP, Hansson M, Vener AV. STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem. 2005;280(39):

[95] Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, et al. Photosys‐ tem II core phosphorylation and photosynthetic acclimation require two different

[96] Tikkanen M, Nurmi M, Kangasjarvi S, Aro EM. Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta.

[97] Herbstova M, Tietz S, Kinzel C, Turkina MV, Kirchhoff H. Architectural switch in plant photosynthetic membranes induced by light stress. Proc Natl Acad Sci U S A.

[98] Nixon PJ, Barker M, Boehm M, de Vries R, Komenda J. FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot. 2005;56(411):357–363.

[99] Barber.J Influence of surface charges on thylakoid structure and function. Annu Rev

[100] Merchant S, Bogorad L. Metal ion regulated gene expression: use of a plastocyanin-less mutant of Chlamydomonas reinhardtii to study the Cu(II)-dependent expression of

[101] Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, et al. Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. Embo J.

[102] Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, et al. Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci U S A. 2003;100(26):16119–16124.

the assembly and repair of photosystem II. Ann Bot. 2010;106(1):1–16.

damage and turnover. Biochim Biophys Acta. 1993;1143(2):113–134.

Nature. 2015;524(7565):366–369.

48 Applied Photosynthesis - New Progress

Acad Sci U S A. 2014;111(44):15839–15844.

protein kinases. Nature. 2005;437(7062):1179–1182.

33679–33686. Epub 2005 Jul 22.

2008;1777(11):1432–1437.

2012;109(49):20130–20135.

Plant Physiol. 1982;33:261–295.

2002;21(24):6709–6720.

cytochrome c-552. EMBO J. 1987;6(9):2531–2535.


[128] Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K. FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2001;98(22):12826–12831.

[115] Yildiz FH, Davies JP, Grossman AR. Characterization of sulfate transport in Chlamy‐ domonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol.

[116] Davies JP, Yildiz F, Grossman AR. Mutants of Chlamydomonas with aberrant respons‐

[117] Wykoff DD, Davies JP, Melis A, Grossman AR. The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant

[118] Melis A, Zhang L, Forestier M, Ghirardi ML, Seibert M. Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green

[119] Woodson JD, Chory J. Organelle signaling: how stressed chloroplasts communicate

[120] Johanningmeier U, Howell SH. Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of

[121] Strand A, Asami T, Alonso J, Ecker JR, Chory J. Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature. 2003;421(6918):79–83.

[122] Mochizuki N, Tanaka R, Tanaka A, Masuda T, Nagatani A. The steady-state level of Mg-protoporphyrin IX is not a determinant of plastid-to-nucleus signaling in Arabi‐ dopsis. Proc Natl Acad Sci U S A. 2008;105(39):15184–15189. Epub 2008 Sep 25.

[123] Moulin M, McCormac AC, Terry MJ, Smith AG. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mg-protopor‐ phyrin IX accumulation. Proc Natl Acad Sci U S A. 2008;105(39):15178–15183. Epub

[124] Kropat J, Oster U, Rudiger W, Beck CF. Chlorophyll precursors are signals of chloro‐ plast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci

[125] Kropat J, Oster U, Rudiger W, Beck CF. Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their

[126] von Gromoff ED, Alawady A, Meinecke L,Grimm B, Beck CF. Heme, a plastid-derived regulator of nuclear gene expression in Chlamydomonas. Plant Cell. 2008;20(3):552–

[127] Voss B, Meinecke L,Kurz T, Al-Babili S, Beck CF, Hess WR. Hemin and magnesiumprotoporphyrin IX induce global changes in gene expression in Chlamydomonas

accessibility to cytoplasm/nucleus. Plant J. 2000;24(4):523–531.

reinhardtii. Plant Physiol. 2011;155(2):892–905.

chlorophyll synthesis precursors. J Biol Chem. 1984;259(21):13541–13549.

alga Chlamydomonas reinhardtii. Plant Physiol. 2000;122(1):127–136.

es to sulfur deprivation. Plant Cell. 1994;6(1):53–63.

with the nucleus. Curr Biol. 2012;22(17):R690–R692.

1994;104(3):981–987.

50 Applied Photosynthesis - New Progress

2008 Sep 25.

567.

U S A. 1997;94(25):14168–14172.

Physiol. 1998;117(1):129–139.


encoded LHCII mRNAs in Chlamydomonas. Proc Natl Acad Sci U S A. 2009;106(32): 13290–13295.

