Skip to main content

Advertisement

Log in

The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses

  • Review Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Plants convert light energy from the sun into chemical energy by photosynthesis. Since they are sessile, they have to deal with a wide range of conditions in their immediate environment. Many abiotic and biotic parameters exhibit considerable fluctuations which can have detrimental effects especially on the efficiency of photosynthetic light harvesting. During evolution, plants, therefore, evolved a number of acclimation processes which help them to adapt photosynthesis to such environmental changes. This includes protective mechanisms such as excess energy dissipation and processes supporting energy redistribution, e.g. state transitions or photosystem stoichiometry adjustment. Intriguingly, all these responses are triggered by photosynthesis itself via the interplay of its light reaction and the Calvin–Benson cycle with the residing environmental condition. Thus, besides its primary function in harnessing and converting light energy, photosynthesis acts as a sensing system for environmental changes that controls molecular acclimation responses which adapt the photosynthetic function to the environmental change. Important signalling parameters directly or indirectly affected by the environment are the pH gradient across the thylakoid membrane and the redox states of components of the photosynthetic electron transport chain and/or electron end acceptors coupled to it. Recent advances demonstrate that these signals control post-translational modifications of the photosynthetic protein complexes and also affect plastid and nuclear gene expression machineries as well as metabolic pathways providing a regulatory framework for an integrated response of the plant to the environment at all cellular levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

Chl:

Chlorophyll

CP:

Chloroplast

CSK:

Chloroplast sensor kinase

Cyt b 6 f :

Cytochrome b 6 f complex

FTR:

Ferredoxin–thioredoxin oxidoreductase

LHC:

Light-harvesting systems

LHCIIb:

The major light-harvesting chlorophyll a/b complexes of photosystem II

LTR:

Long-term response

PAR:

Photosynthetic active radiation

PEP:

Plastid encoded RNA polymerase

P-LHCIIb:

Phosphorylated LHCIIb

PQ:

Plastoquinone

PS:

Photosystem

PTK:

Plastid transcription kinase

RC:

Reaction centre

RubisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SIG1:

Sigma factor 1

References

  • Allen JF (1993) Control of gene-expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J Theor Biol 165:609–631

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2003) State transitions—a question of balance. Science 299:1530–1532

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2005a) Photosynthesis: the processing of redox signals in chloroplasts. Curr Biol 15:R929–R932

    Article  PubMed  CAS  Google Scholar 

  • Allen JF (2005b) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett 579:963–968

    Article  PubMed  CAS  Google Scholar 

  • Allen JF, Pfannschmidt T (2000) Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Philos T Roy Soc B 355(1402):1351–1357

    Article  CAS  Google Scholar 

  • Amunts A, Nelson N (2009) Plant photosystem I design in the light of evolution. Structure 17:637–650

    Article  PubMed  CAS  Google Scholar 

  • Anderson JM, Chow WS, Park Y-I (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

    Article  CAS  Google Scholar 

  • Arnon DI (1982) Sunlight, earth, life: the grand design of photosynthesis. Sciences 22:22–27

    Google Scholar 

  • Aro E-M, Andersson B (2001) Regulation of photosynthesis. Advances in photosynthesis and respiration, vol 11. Kluwer Academic, Dordrecht

    Google Scholar 

  • Aro EM, Ohad I (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid Redox Sign 5:55–67

    Article  CAS  Google Scholar 

  • Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515

    Article  PubMed  CAS  Google Scholar 

  • Baena-Gonzalez E (2010) Energy signaling in the regulation of gene expression during stress. Mol Plant 3:300–313

    Article  PubMed  CAS  Google Scholar 

  • Baena-Gonzalez E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Philos T Roy Soc B 357:1451–1459

    Article  CAS  Google Scholar 

  • Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34:619–631

    Article  PubMed  CAS  Google Scholar 

  • Barzda V, Istokovics A, Simidjiev I, Garab G (1996) Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment–protein complexes. Light-induced reversible structural changes associated with energy dissipation. Biochemistry 35:8981–8985

    Article  PubMed  CAS  Google Scholar 

  • Bassi R, Caffarri S (2000) Lhc proteins and the regulation of photosynthetic light harvesting function by xanthophylls. Photosynth Res 64:243–256

    Article  PubMed  CAS  Google Scholar 

  • Bellafiore S, Bameche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase Stn7. Nature 433:892–895

    Article  PubMed  CAS  Google Scholar 

  • Blankenship RE (2002) Molecular regulation of photosynthesis. Blackwell Science, Oxford

    Book  Google Scholar 

  • Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182

    Article  PubMed  CAS  Google Scholar 

  • Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–389

    Article  PubMed  CAS  Google Scholar 

  • Bräutigam K, Dietzel L, Kleine T, Ströher E, Wormuth D, Dietz KJ, Radke D, Wirtz M, Hell R, Dörmann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T (2009) Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21:2715–2732

    Article  PubMed  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    Article  PubMed  CAS  Google Scholar 

  • Buchanan BB, Gruissem W, Jones RL (2002) Biochemistry and molecular biology of plants. Wiley, Somerset

    Google Scholar 

  • Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M (2009) Copper homeostasis. New Phytol 182:799–816

    Article  PubMed  CAS  Google Scholar 

  • Caffarri S, Kouril R, Kereiche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II super-complexes. EMBO J 28:3052–3063

    Article  PubMed  CAS  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  PubMed  CAS  Google Scholar 

  • Chow WS, Melis A, Anderson JM (1990) Adjustments of photosystem stoichiometry in chloroplasts improve the quantum efficiency of photosynthesis. Proc Natl Acad Sci USA 87:7502–7506

    Article  PubMed  CAS  Google Scholar 

  • Dall'Osto L, Cazzaniga S, North H, Marion-Poll A, Bassi R (2007) The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19:1048–1064

    Article  PubMed  CAS  Google Scholar 

  • Dekker JP, van Roon H, Boekema EJ (1999) Heptameric association of light-harvesting complex II trimers in partially solubilized photosystem II membranes. FEBS Lett 449:211–214

    Article  PubMed  CAS  Google Scholar 

  • Depege N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485

    Article  PubMed  CAS  Google Scholar 

  • Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry—functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Deane JA, Tan S, McFadden GI, Gantt E, Green BR (1999) A phylogenetic assessment of the eukaryotic light-harvesting antenna proteins, with implications for plastid evolution. J Mol Evol 48:59–68

    Article  PubMed  CAS  Google Scholar 

  • Durnford DG, Price JA, McKim SM, Sarchfield ML (2003) Light-harvesting complex gene expression is controlled by both transcriptional and post-transcriptional mechanisms during photoacclimation in Chlamydomonas reinhardtii. Physiol Plant 118:193–205

    Article  CAS  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  PubMed  CAS  Google Scholar 

  • Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44

    Article  CAS  Google Scholar 

  • Fey V, Wagner R, Brautigam K, Pfannschmidt T (2005a) Photosynthetic redox control of nuclear gene expression. J Exp Bot 56:1491–1498

    Article  PubMed  CAS  Google Scholar 

  • Fey V, Wagner R, Brautigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmuller R, Pfannschmidt T (2005b) Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J Biol Chem 280:5318–5328

    Article  PubMed  CAS  Google Scholar 

  • Garab G, Faludi-Daniel A, Sutherland JC, Hind G (1988) Macro-organization of chlorophyll a/b light-harvesting complex in thylakoids and aggregates: information from circular differential scattering. Biochemistry 27:2425–2430

    Article  CAS  Google Scholar 

  • Georgakopoulou S, van der Zwan G, Bassi R, van Grondelle R, van Amerongen H, Croce R (2007) Understanding the changes in the circular dichroism of light harvesting complex II upon varying its pigment composition and organization. Biochemistry 46:4745–4754

    Article  PubMed  CAS  Google Scholar 

  • Ghannoum O (2009) C(4) photosynthesis and water stress. Ann Bot 103:635–644

    Article  PubMed  CAS  Google Scholar 

  • Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    Article  PubMed  CAS  Google Scholar 

  • Herrmann RG, Maier RM, Schmitz-Linneweber C (2003) Eukaryotic genome evolution: rearrangement and co-evolution of compartmentalized genetic information. Philos T Roy Soc B 358:87–97

    Article  CAS  Google Scholar 

  • Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of non-photochemical quenching in green plants. Biochemistry 43:8281–8289

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Rees D, Pascal AA, Noctor G, Young AJ (1991) Control of the light-harvesting function of chloroplast membranes by aggregation of the LHCII chlorophyll protein complex. FEBS Lett 292:1–4

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Murchie EH, Ruban AV, Walters RG (2001) Increasing rice photosynthesis by manipulation of the acclimation and adaptation to light. In: Rice biotechnology: improving yield, stress tolerance and grain quality, vol 236. Novartis Foundation Symposium. pp 117-134

  • Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275(6):1069–1079

    Article  PubMed  CAS  Google Scholar 

  • Huner NPA, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Istokovics A, Simidjiev I, Lajko F, Garab G (1997) Characterization of the light induced reversible changes in the chiral macro-organization of the chromophores in chloroplast thylakoid membranes. Temperature dependence and effect of inhibitors. Photosynth Res 54:45–53

    Article  CAS  Google Scholar 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4(6):236–240

    Article  PubMed  Google Scholar 

  • Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochim Biophys Acta 1807:384–389

    Article  PubMed  CAS  Google Scholar 

  • Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283–289

    Article  PubMed  CAS  Google Scholar 

  • Kanervo E, Suorsa M, Aro EM (2005) Functional flexibility and acclimation of the thylakoid membrane. Photochem Photobiol Sci 4:1072–1080

    Article  PubMed  CAS  Google Scholar 

  • Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 9:627–640

    PubMed  CAS  Google Scholar 

  • Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

    Article  PubMed  CAS  Google Scholar 

  • Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978

    Article  PubMed  CAS  Google Scholar 

  • Kolbe A, Oliver SN, Fernie AR, Stitt M, van Dongen JT, Geigenberger P (2006) Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thiol-disulfide status on plant metabolism. Plant Physiol 141:412–422

    Article  PubMed  CAS  Google Scholar 

  • Kouril R, Oostergetel GT, Boekema EJ (2011) Fine structure of granal thylakoid membrane organization using cryo electron tomography. Biochim Biophys Acta 1807:368–374

    Article  PubMed  CAS  Google Scholar 

  • Koziol AG, Borza T, Ishida KI, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816

    Article  PubMed  CAS  Google Scholar 

  • Lambrev PH, Schmitt FJ, Kussin S, Schoengen M, Varkonyi Z, Eichler HJ, Garab G, Renger G (2011) Functional domain size in aggregates of light-harvesting complex II and thylakoid membranes. Biochim Biophys Acta 1807:1022–1031

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW, Tezara W (2009) Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 103:561–579

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi K (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

    Article  PubMed  CAS  Google Scholar 

  • Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the psbs protein. J Biol Chem 279:22866–22874

    Article  PubMed  CAS  Google Scholar 

  • Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR (2004) Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution. Nature 428:287–292

    Article  PubMed  CAS  Google Scholar 

  • Liu C, Zhang Y, Cao D, He Y, Kuang T, Yang C (2008) Structural and functional analysis of the antiparallel strands in the lumenal loop of the major light-harvesting chlorophyll a/b complex of photosystem II (LHCIIb) by site-directed mutagenesis. J Biol Chem 283:487–495

    Article  PubMed  CAS  Google Scholar 

  • Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330

    Article  PubMed  CAS  Google Scholar 

  • Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, Leister D, Stoebe B, Hasegawa M, Penny D (2002) Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci USA 99:12246–12251

    Article  PubMed  CAS  Google Scholar 

  • Melkozernov AN, Barber J, Blankenship RE (2006) Light harvesting in photosystem I supercomplexes. Biochemistry 45:331–345

    Article  PubMed  CAS  Google Scholar 

  • Miloslavina Y, Wehner A, Lambrev PH, Wientjes E, Reus M, Garab G, Croce R, Holzwarth AR (2008) Far-red fluorescence: a direct spectroscopic marker for LHCII oligomer formation in non-photochemical quenching. FEBS Lett 582:3625–3631

    Article  PubMed  CAS  Google Scholar 

  • Mishra Y, Johanssons-Jankanpaa H, Kiss AZ, Funk C, Schroder WP, Jansson S (2012) Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components. BMC Plant Biol 12:6

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  PubMed  CAS  Google Scholar 

  • Moya I, Silvestri M, Vallon O, Cinque G, Bassi R (2001) Time-resolved fluorescence analysis of the photosystem II antenna proteins in detergent micelles and liposomes. Biochemistry 40:12552–12561

    Article  PubMed  CAS  Google Scholar 

  • Mullineaux CW, Pascal AA, Horton P, Holzwarth AR (1993) Excitation-energy quenching in aggregates of the LHC-II chlorophyll–protein complex—a time-resolved fluorescence study. Biochim Biophys Acta 1141:23–28

    Article  CAS  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251

    Article  PubMed  CAS  Google Scholar 

  • Murchie EH, Pinto M, Horton P (2009) Agriculture and the new challenges for photosynthesis research. New Phytol 181:532–552

    Article  PubMed  CAS  Google Scholar 

  • Nathan N (2011) Photosystems and global effects of oxygenic photosynthesis. Biochim Biophys Acta 1807:856–863

    Article  CAS  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  PubMed  CAS  Google Scholar 

  • Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382

    Article  PubMed  CAS  Google Scholar 

  • Novoderezhkin VI, Palacios MA, van Amerongen H, van Grondelle R (2005) Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2.72 angstrom crystal structure. J Phys Chem 109:10493–10504

    CAS  Google Scholar 

  • Oswald O, Martin T, Dominy PJ, Graham IA (2001) Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. Proc Natl Acad Sci USA 98:2047–2052

    Article  PubMed  CAS  Google Scholar 

  • Parry MAJ, Reynolds M, Salvucci ME, Raines C, Andralojc PJ, Zhu X, Price GD, Condon AG, Furbank RT (2011) Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J Exp Bot 62:453–467

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: the roles of Stn7, Stn8 and Tap38. Biochim Biophys Acta 1807:887–896

    Article  PubMed  CAS  Google Scholar 

  • Petracek ME, Dickey LF, Huber SC, Thompson WF (1997) Light-regulated changes in abundance and polyribosome association of ferredoxin mRNA are dependent on photosynthesis. Plant Cell 9:2291–2300

    PubMed  CAS  Google Scholar 

  • Petracek ME, Dickey LF, Nguyen TT, Gatz C, Sowinski DA, Allen GC, Thompson WF (1998) Ferredoxin-1 mRNA is destabilized by changes in photosynthetic electron transport. Proc Natl Acad Sci USA 95:9009–9013

    Article  PubMed  CAS  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R (2006) pTAC2, -6, and -12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41

    Article  PubMed  CAS  Google Scholar 

  • Pfannschmidt T, Nilsson A, Allen JF (1999a) Photosynthetic control of chloroplast gene expression. Nature 397:625–628

    Article  CAS  Google Scholar 

  • Pfannschmidt T, Nilsson A, Tullberg A, Link G, Allen JF (1999b) Direct transcriptional control of the chloroplast genes psbA and psaAB adjusts photosynthesis to light energy distribution in plants. IUBMB Life 48:271–276

    PubMed  CAS  Google Scholar 

  • Piippo M, Allahverdiyeva Y, Paakkarinen V, Suoranta UM, Battchikova N, Aro EM (2006) Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol Genomics 25:142–152

    Article  PubMed  CAS  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinchi E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, Van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc Natl Acad Sci USA 105:10061–10066

    Article  PubMed  CAS  Google Scholar 

  • Puthiyaveetil S, Ibrahim IM, Jelicic B, Tomasic A, Fulgosi H, Allen JF (2010) Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biol Evol 2:888–896. doi:10.1093/gbe/evq073

    Article  PubMed  Google Scholar 

  • Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807:375–383

    Article  PubMed  CAS  Google Scholar 

  • Romanowska E, Kargul J, Powikrowska M, Finazzi G, Nield J, Drozak A, Pokorska B (2008) Structural organization of photosynthetic apparatus in agranal chloroplasts of maize. J Biol Chem 283:26037–26046

    Article  PubMed  CAS  Google Scholar 

  • Ruban AV, Johnson MP (2010) Xanthophylls as modulators of membrane protein function. Arch Biochem Biophys 504:78–85

    Article  PubMed  CAS  Google Scholar 

  • Schroter Y, Steiner S, Matthai K, Pfannschmidt T (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics 10:2191–2204

    Article  PubMed  CAS  Google Scholar 

  • Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1274

    Article  PubMed  Google Scholar 

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation anate transitions in Arabidopsis. Proc Natl Acad Sci USA 107:4782–4787

    Article  PubMed  CAS  Google Scholar 

  • Shcolnick S, Keren N (2006) Metal homeostasis in cyanobacteria and chloroplasts. Balancing benefits and risks to the photosynthetic apparatus. Plant Physiol 141:805–810

    Article  PubMed  CAS  Google Scholar 

  • Sheramati I, Nakamura M, Yamamoto YY, Pfannschmidt T, Obokata J, Oelmuller R (2002) Polyribosome loading of spinach mRNAs for photosystem I subunits is controlled by photosynthetic electron transport—a crucial cis element in the spinach PsaD gene is located in the 5′-untranslated region. Plant J 32:631–639

    Article  Google Scholar 

  • Shimizu M, Kato H, Ogawa T, Kurachi A, Nakagawa Y, Kobayashi H (2010) Sigma factor phosphorylation in the photosynthetic control of photosystem stoichiometry. Proc Natl Acad Sci USA 107:10760–10764

    Article  PubMed  CAS  Google Scholar 

  • Standfuss J, van Scheltinga ACT, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and non-photochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J 24:919–928

    Article  PubMed  CAS  Google Scholar 

  • Steiner S, Dietzel L, Schröter Y, Fey V, Wagner R, Pfannschmidt T (2009) The role of phosphorylation in redox regulation of photosynthesis genes psaA and psbA during photosynthetic acclimation of mustard. Mol Plant 2:416–429

    Article  PubMed  CAS  Google Scholar 

  • Stoebe B, Maier UG (2002) One, two, three: nature's tool box for building plastids. Protoplasma 219:123–130

    Article  PubMed  Google Scholar 

  • Szabo I, Bergantino E, Giacometti GM (2005) Light and oxygenic photosynthesis: energy dissipation as a protection mechanism against photo-oxidation. EMBO Rep 6:629–634

    Article  PubMed  CAS  Google Scholar 

  • Szabo M, Lepetit B, Goss R, Wilhelm C, Mustardy L, Garab G (2008) Structurally flexible macro-organization of the pigment–protein complexes of the diatom Phaeodactylum tricornutum. Photosynth Res 95:237–245

    Article  PubMed  CAS  Google Scholar 

  • Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60

    Article  PubMed  CAS  Google Scholar 

  • Terashima I, Hikosaka K (1995) Comparative ecophysiology of leaf and canopy photosynthesis. Plant Cell Environ 18:1111–1128

    Article  Google Scholar 

  • Tikkanen M, Pippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener A, Allahverdiyeva Y, Aro EM (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793

    Article  PubMed  CAS  Google Scholar 

  • Tiller K, Link G (1993) Phosphorylation and dephosphorylation affect functional-characteristics of chloroplast and etioplast transcription systems from mustard (Sinapis-alba L). EMBO J 12:1745–1753

    PubMed  CAS  Google Scholar 

  • Tullberg A, Alexciev K, Pfannschmidt T, Allen JF (2000) Photosynthetic electron flow regulates transcription of the psaB gene in pea (Pisum sativum L.) chloroplasts through the redox state of the plastoquinone pool. Plant Cell Physiol 41:1045–1054

    Article  PubMed  CAS  Google Scholar 

  • Varkonyi Z, Nagy G, Lambrev P, Kiss AZ, Szekely N, Rosta L, Garab G (2009) Effect of phosphorylation on the thermal and light stability of the thylakoid membranes. Photosynth Res 99:161–171

    Article  PubMed  CAS  Google Scholar 

  • Wagner R, Dietzel L, Bräutigam K, Fischer W, Pfannschmidt T (2008) The long-term response to fluctuating light quality is an important and distinct light acclimation mechanism that supports survival of Arabidopsis thaliana under low light conditions. Planta 228:573–587

    Article  PubMed  CAS  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447

    Article  PubMed  CAS  Google Scholar 

  • Walters RG, Horton P (1994) Acclimation of Arabidopsis-thaliana to the light environment—changes in composition of the photosynthetic apparatus. Planta 195:248–256

    Article  CAS  Google Scholar 

  • Yang DH, Andersson B, Aro EM, Ohad I (2001) The redox state of the plastoquinone pool controls the level of the light-harvesting chlorophyll a/b binding protein complex II (LHC II) during photoacclimation—cytochrome b(6)f deficient Lemna perpusilla plants are locked in a state of high-light acclimation. Photosynth Res 68:163–174

    Article  PubMed  CAS  Google Scholar 

  • Yang CH, Lambrev P, Chen Z, Javorfi T, Kiss AZ, Paulsen H, Garab G (2008) The negatively charged amino acids in the lumenal loop influence the pigment binding and conformation of the major light-harvesting chlorophyll a/b complex of photosystem II. Biochim Biophys Acta 1777:1463–1470

    Article  PubMed  CAS  Google Scholar 

  • Zhao SZ, Qi XQ (2008) Signaling in plant disease resistance and symbiosis. J Integr Plant Biol 50:799–807

    Article  PubMed  CAS  Google Scholar 

  • Zhu X-G, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Work in the laboratories of the authors is supported by grants from the Deutsche Forschungsgemeinschaft (DFG), the Chinese Academy of Science and the National Natural Science Foundation of China (NSFC).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Thomas Pfannschmidt or Chunhong Yang.

Additional information

Handling Editor: Peter Nick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pfannschmidt, T., Yang, C. The hidden function of photosynthesis: a sensing system for environmental conditions that regulates plant acclimation responses. Protoplasma 249 (Suppl 2), 125–136 (2012). https://doi.org/10.1007/s00709-012-0398-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-012-0398-2

Keywords

Navigation