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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

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Abstract

The long-term response (LTR) of higher plants to varying light qualities increases the photosynthetic yield; however, the benefit of this improvement for physiology and survival of plants is largely unknown, and its functional relation to other light acclimation responses has never been investigated. To unravel positive effects of the LTR we acclimated Arabidopsis thaliana for several days to light sources, which preferentially excite photosystem I (PSI) or photosystem II (PSII). After acclimation, plants revealed characteristic differences in chlorophyll fluorescence, thylakoid membrane stacking, phosphorylation state of PSII subunits and photosynthetic yield of PSII and PSI. These LTR-induced changes in the structure, function and efficiency of the photosynthetic machinery are true effects by light quality acclimation, which could not be induced by light intensity variations in the low light range. In addition, high light stress experiments indicated that the LTR is not involved in photoinhibition; however, it lowers non-photochemical quenching (NPQ) by directing more absorbed light energy into photochemical work. NPQ in turn is not essential for the LTR, since npq mutants performed a normal acclimation. We quantified the beneficial potential of the LTR by comparing wild-type plants with the LTR-deficient mutant stn7. The mutant exhibited a decreased effective quantum yield and produced only half of seeds when grown under fluctuating light quality conditions. Thus, the LTR represents a distinct acclimation response in addition to other already known responses that clearly improves plant physiology under low light conditions resulting in a pronounced positive effect on plant fitness.

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Abbreviations

Chl:

Chlorophyll

LHC:

Light-harvesting complex

LTR:

Long-term response

NPQ:

Non-photochemical quenching

PS:

Photosystem

PQ:

Plastoquinone

WT:

Wild-type

References

  • Alfonso M, Perewoska I, Constant S, Kirilovsky D (1999) Redox control of psbA expression in cyanobacteria Synechocystis strains. J Photochem Photobiol 48:104–113

    Article  CAS  Google Scholar 

  • Allen JF (1995) Thylakoid protein-phosphorylation, state-1-state-2 transitions, and photosystem stoichiometry adjustment—redox control at multiple levels of gene-expression. Physiol Plant 93:196–205

    Article  CAS  Google Scholar 

  • Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6:317–326

    Article  PubMed  CAS  Google Scholar 

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen HM, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  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 

  • Andrews JR, Bredenkamp GJ, Baker NR (1993) Evaluation of the role of state transitions in determining the efficiency of light utilisation for CO2 assimilation in leaves. Photosynth Res 38:15–26

    Article  CAS  Google Scholar 

  • Aro EM, Andersson B (2001) Regulation of photosynthesis. Kluwer, Dordrecht

    Google Scholar 

  • Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801

    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 mechanisms of photosynthesis. Blackwell Science, Oxford

    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 

  • Bräutigam K, Dietzel L, Pfannschmidt T (2007) Plastid-nucleus communication: anterograde and retrograde signalling in development and function of plastids. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 409–455

    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 

  • Deng XW, Tonkyn JC, Peter GF, Thornber JP, Gruissem W (1989) Post-transcriptional control of plastid messenger-RNA accumulation during adaptation of chloroplasts to different light quality environments. Plant Cell 1:645–654

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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 

  • Frenkel M, Bellafiore S, Rochaix JD, Jansson S (2007) Hierarchy amongst photosynthetic acclimation responses for plant fitness. Physiol Plant 129:455–459

    Article  CAS  Google Scholar 

  • Frigerio S, Campoli C, Zorzan S, Fantoni LI, Crosatti C, Drepper F, Haehnel W, Cattivelli L, Morosinotto T, Bassi R (2007) Photosynthetic antenna size in higher plants is controlled by the plastoquinone redox state at the post-transcriptional rather than transcriptional level. J Biol Chem 282:29457–29469

    Article  PubMed  CAS  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305

    Article  PubMed  CAS  Google Scholar 

  • Jiao YL, Lau OS, Deng XW (2007) Light-regulated transcriptional networks in higher plants. Nat Rev Genet 8:217–230

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Glick RE, Melis A (1993) Dynamics of photosystem stoichiometry adjustment by light quality in chloroplasts. Plant Physiol 102:181–190

    PubMed  CAS  Google Scholar 

  • Klughammer C, Schreiber U (1998) Measuring P700 absorbance changes in the near infrared spectral region with a dual wavelength pulse modulation system. In: Govindjee (ed) Photosynthesis: mechanisms and effects. Kluwer, Dordrecht, pp 4357–4360

    Google Scholar 

  • Kovacs L, Wiessner W, Kis M, Nagy F, Mende D, Demeter S (2000) Short- and long-term redox regulation of photosynthetic light energy distribution and photosystem stoichiometry by acetate metabolism in the green alga, Chlamydobotrys stellata. Photosynth Res 65:231–247

    Article  PubMed  CAS  Google Scholar 

  • Kovacs L, Damkjaer J, Kereiche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120

    Article  PubMed  CAS  Google Scholar 

  • Kruk J, Karpinski S (2005) Redox state analysis of the plastoquinone pool in Arabidopsis thaliana reveals unexpected changes under different light conditions. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects of global perspectives. 13th international congress of photosynthesis. Montreal, pp 568–570

  • Kruk J, Karpinski S (2006) An HPLC-based method of estimation of the total redox state of plastoquinone in chloroplasts, the size of the photochemically active plastoquinone-pool and its redox state in thylakoids of Arabidopsis. Biochim Biophys Acta Bioenerg 1757:1669–1675

    Article  CAS  Google Scholar 

  • Kruse O (2001) Light-induced short-term adaptation mechanisms under redox control in the PSII-LHCII supercomplex: LHC II state transitions and PSII repair cycle. Naturwissenschaften 88:284–292

    Article  PubMed  CAS  Google Scholar 

  • Kulheim C, Agren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93

    Article  PubMed  Google Scholar 

  • Li H, Sherman LA (2000) A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp strain PCC 6803. J Bacteriol 182:4268–4277

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • Melis A (1991) Dynamics of photosynthetic membrane composition and function. Biochim Biophys Acta 1058:87–106

    Article  CAS  Google Scholar 

  • Melis A, Harvey GW (1981) Regulation of photosystem stoichiometry, chlorophyll-a and chlorophyll-b content and relation to chloroplast ultrastructure. Biochim Biophys Acta 637:138–145

    Article  CAS  Google Scholar 

  • Mullineaux CW, Emlyn-Jones D (2005) State transitions: an example of acclimation to low-light stress. J Exp Bot 56:389–393

    Article  PubMed  CAS  Google Scholar 

  • Murakami A, Fujita Y, Nemson JA, Melis A (1997) Chromatic regulation in Chlamydomonas reinhardtii: time course of photosystem stoichiometry adjustment following a shift in growth light quality. Plant Cell Physiol 38:188–193

    CAS  Google Scholar 

  • Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Pesaresi P, Schneider A, Kleine T, Leister D (2007) Interorganellar communication. Curr Opin Plant Biol 10:600–606

    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 (1999) Photosynthetic control of chloroplast gene expression. Nature 397:625–628

    Article  CAS  Google Scholar 

  • Pfannschmidt T, Allen JF, Oelmuller R (2001a) Principles of redox control in photosynthesis gene expression. Physiol Plant 112:1–9

    Article  CAS  Google Scholar 

  • Pfannschmidt T, Schutze K, Brost M, Oelmuller R (2001b) A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment. J Biol Chem 276:36125–36130

    Article  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 Genom 25:142–152

    Article  CAS  Google Scholar 

  • Pons T, de Jong-Van Berkel Y (2004) Species-specific variation in the importance of the spectral quality gradient in canopies as a signal for photosynthetic resource partitioning. Ann Bot 94:725–732

    Article  PubMed  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents—verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Rintamaki E, Salonen M, Suoranta UM, Carlberg I, Andersson B, Aro EM (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo—application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem 272:30476–30482

    Article  PubMed  CAS  Google Scholar 

  • Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Bilger W, Hormann H, Neubauer C (1997) Chlorophyll fluorescence as a diagnostic tool: basics and some aspects of practical relevance. In: Raghavendra AS (ed) Photosynthesis: a comprehensive treatise. Cambridge University Press, Cambridge, pp 320–336

    Google Scholar 

  • Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591

    Article  PubMed  CAS  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Takemiya A, Inoue S, Doi M, Kinoshita T, Shimazaki K (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120–1127

    Article  PubMed  CAS  Google Scholar 

  • Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, 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  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 

  • Vainonen JP, Hansson M, Vener AV (2005) STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 280:33679–33686

    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 

  • Walters RG, Rogers JJM, Shephard F, Horton P (1999) Acclimation of Arabidopsis thaliana to the light environment: the role of photoreceptors. Planta 209:517–527

    Article  PubMed  CAS  Google Scholar 

  • Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the DFG to TP and the DFG research groups FOR 387, FOR 804 and by the NWP programme of Thuringia. Meta Brost and Nicole Manthei are acknowledged for their skilful technical assistance.

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Authors and Affiliations

  1. Junior Research Group, Institute for General Botany and Plant Physiology, Friedrich-Schiller-University Jena, Dornburger Str. 159, 07743, Jena, Germany

    Raik Wagner, Lars Dietzel, Katharina Bräutigam & Thomas Pfannschmidt

  2. Research Group Limnology, Institute for Ecology, Friedrich-Schiller-University Jena, Dornburger Str. 159, 07743, Jena, Germany

    Wolfgang Fischer

Authors
  1. Raik Wagner
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  2. Lars Dietzel
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  3. Katharina Bräutigam
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  4. Wolfgang Fischer
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  5. Thomas Pfannschmidt
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Correspondence to Thomas Pfannschmidt.

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Raik Wagner and Lars Dietzel contributed equally to this article.

Electronic supplementary material

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425_2008_760_MOESM1_ESM.pdf

MOESM1 [Fig. S1 PAM measurements under PSII light with addition of PSI light. The fluorescence trace reveals the oxidising effect of the PSI light source. Plants grown under white light were subjected to the PSII light source (PAR: 24 μmol photons m-2 s-1) and supplemented with PSI light of 12 μmol photons m-2 s-1 for approx. 15 minutes. Then the PSI light source was turned off resulting in a rise of steady state fluorescence. Turning it on again after ca. 10 min, consequently, led to the contrary effect. The difference in the height of the initial rise of fluorescence and the drop of fluorescence at the end of the experiment can be ascribed to state transitions] (PDF 163 kb)

425_2008_760_MOESM2_ESM.pdf

MOESM2 [Fig. S2 Chl fluorescence kinetics of Arabidopsis thaliana WT using PSI- or PSII-light sources as actinic light. The schemes show typical Chl fluorescence traces obtained with PSI or PSII plants as shown in Fig. 2. In this experiments the intensity of the light sources was adjusted in such a way that it was either 20 µmol photons m-2 s-1 for PSI-light and 10 µmol photons m-2 s-1 for PSII-light or vice versa. The light source used for respective illumination of plants is indicated by an arrow below the traces. Upward arrow: light on; downward arrow: light off. Note the strong oxidizing effect of the PSI-light source which occurs regardless of its intensity as it becomes visible by the much lower steady state fluorescence in comparison to PSII-light. Full oxidation of the electron transport chain was achieved by intermittent illumination of the plants with a far-red light diode] (PDF 2774 kb)

425_2008_760_MOESM3_ESM.pdf

MOESM3 [Fig. S3 PSI activity determined by P700 absorbance changes. Typical far-red absorption curves of P700 from differentially acclimated plants are shown in relative absorption units. The growth light condition is indicated in the upper left corner of each diagramme. fr, actinic far-red light; sp, saturating white light pulse] (PDF 580 kb)

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Wagner, R., Dietzel, L., Bräutigam, K. et al. 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 (2008). https://doi.org/10.1007/s00425-008-0760-y

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