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Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis

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Abstract

Global transcriptome analyses were used to assess the interactive effects of short-term stress versus long-term acclimation to high light (HL), low temperature (LT) and excitation pressure in Arabidopsis. Microarray analyses indicated that exposure to stress resulted in two times as many modulated transcripts in both, high-light-treated and low-temperature-treated plants, compared to plants that were fully acclimated to either one of these conditions. We showed that 10.9 % of all transcripts were regulated in the same way by both stress conditions, and hence, were categorized as excitation pressure regulated, rather than regulated by either high-light or low-temperature stress per se. This group of chloroplast redox-sensitive genes included various photosynthetic genes as well as genes known to be associated with cold acclimation (cbf3, cor15A, cor15B) and gibberellic acid (GA) metabolism and signalling (ga2ox1, gai). Chemical inhibition of the photosynthetic electron transport by either DCMU or DBMIB indicated that although the plastoquinone pool contributes significantly to redox regulation of the transcriptome (8.6 %), it appears that PSI represents the major source of redox signals (89 %), whereas PSII appears to contribute only 3.1 %. A comparison of the gene expression profiles between stress and acclimated plants indicated that 10 % of the genes induced by a short, 1-h stress were also associated with long-term acclimation to high excitation pressure. This included the APETALA2/ETHYLENE-RESPONSIVE-BINDING PROTEIN family, the MYB domain- and MYB-related transcription factor family as well as the GRAS transcription factor family important in GA signalling confirming that acclimation to stress is a time-nested phenomenon. We suggest that acclimation to photosynthetic redox imbalance extends beyond the chloroplast and the leaf cell to systemic ROS signalling. This is discussed in terms of the control of plant phenotype through regulation of the nuclear encoded cbf regulon and GA metabolism.

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Abbreviations

Chl:

Chlorophyll

Cyt b6/f :

Cytochrome b6/f

DBMIB:

2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

Fo :

Minimum yield of chlorophyll fluorescence in open PSII centres

F v/F m :

Maximum photochemical efficiency of PSII in the dark-adapted state

GA:

Gibberellic acid

LHCII a/b :

Light-harvesting chlorophyll a/b-protein complex of PSII

P700:

Reaction centre chlorophyll of PSI

PQ:

Plastoquinone

PSI:

Photosystem I

PSII:

Photosystem II

qN:

Non-photochemical quenching

qP:

Photochemical quenching parameter

QA :

Primary electron-accepting quinone in PSII

Q B :

Secondary electron-accepting quinone in PSII

ROS:

Reactive oxygen species

References

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

    Article  CAS  PubMed  Google Scholar 

  • Anderson J (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136

    Article  CAS  Google Scholar 

  • Anderson J, 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  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Heber U, Schreiber U (1993) Electron flow to the intersystem chain from stromal and cyclic electron flow in maize chloroplasts as detected in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol 34:39–50

    CAS  Google Scholar 

  • Baker NR (1991) A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570

    Article  CAS  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Brautigam K, Dietzel L, Kleine T, Stroher E, Wormuth D, Dietz K-J, Radke D, Wirtz M, Hell R, Dormann 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  PubMed Central  Google Scholar 

  • Chi W, Sun X, Zhang L (2013) Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol 64:559–582

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Chory J (1997) Light modulation of vegetative development. Plant Cell 9:1225–1234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Claeys H, Van Landeghem S, Dubois M, Maleux K, Inze D (2014) What Is Stress? Dose-response effects in commonly used in vitro stress assays. Plant Physiol 165:519–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dahal K, Gadapati W, Savitch L, Singh J, Hüner NPA (2012) Cold acclimation and BnCBF17-over-expression enhance photosynthetic performance and energy conversion efficiency during long-term growth of Brassica napus under elevated CO2 conditions. Planta 236:1639–1652

    Article  CAS  PubMed  Google Scholar 

  • Dahal K, Knowles VL, Plaxton WC, Hüner NPA (2014) Enhancement of photosynthetic performance, water use efficiency and grain yield during long-term growth under elevated CO2 in wheat and rye is growth temperature and cultivar dependent. Environ Exp Bot 106:207–220

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Derks A, Shaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468

    Article  CAS  PubMed  Google Scholar 

  • Dietz K-J (2015) Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J Exp Bot 66:2401–2414

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz K-J, Schreiber U, Heber U (1985) The relationship between the redox state of QA and photosynthesis in leaves at various carbon-dioxide, oxygen and light regimes. Planta 166:219–226

    Article  CAS  PubMed  Google Scholar 

  • Durnford DG, Falkowski PG (1997) Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth Res 53:229–241

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Escoubas J-M, Lomas M, LaRoche J, Falkowski PG (1995) Light intensity regulates cab gene transcription via the redox state of the plastoquinone pool in the green alga, Dunaliella tertiolecta. Proc Natl Acad Sci USA 92:10237–10241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falkowski PG, Chen Y-B (2003) Photoacclimation of light harvesting systems in eukaryotic algae. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration. Light harvesting systems in photosynthesis, vol 13. Kluwer, Dordrecht, pp 423–427

    Chapter  Google Scholar 

  • Falkowski PG, LaRoche J (1991) Acclimation to spectral irradiance in algae. J Phycol 27:8–14

    Article  Google Scholar 

  • Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, Schafer E, Fu X, Fan L-M, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez AP, Strand A (2008) Retrograde signaling and plant stress: plastid signals initiate cellular stress responses. Curr Opin Plant Biol 11:509–513

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antiox Redox Signal 11:861–905

    Article  CAS  Google Scholar 

  • Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J (2012) Photosynthetic control of electron transport and the regulation of gene expression. J Exp Bot 63:1637–1661

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Murakami A, Aizawa K, Ohki K (1994) Short-term and long-term adaptation of the photosynthetic apparatus: homeostatic properties of thylakoids. In: Bryant DA (ed) The Molecular Biology of Cyanobacteria. Advances in Photosynthesis, vol 1. Kluwer, Dordrecht, pp 667–692

    Google Scholar 

  • Galvez-Valdivieso G, Mullineaux PM (2010) The role of reactive oxygen species in signalling from chloroplasts to the nucleus. Physiol Plant 138:430–439

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray GR, Heath D (2005) A global reorganization of the metabolome in Arabidopsis during cold acclimation is revealed by metabolic fingerprinting. Physiol Plant 124:236–248

    Article  CAS  Google Scholar 

  • Gray GR, Savitch LV, Ivanov AG, Hüner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110:61–71

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray GR, Chauvin L-P, Sarhan F, Hüner NPA (1997) Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiol 114:467–474

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    Article  CAS  Google Scholar 

  • Guy C, Porat R, Hurry V (2006) Plant cold and abiotic stress gets hot. Physiol Plant 126:1–4

    Article  CAS  Google Scholar 

  • Hedden P (2003) The genes of the green revolution. Trends Genet 19:5–9

    Article  CAS  PubMed  Google Scholar 

  • Holmstrom KM, Finkel T (2014) Cellular mechanisms and physiological consequences of redox-dependent signalling. Nat Rev Mol Cell Biol 15:411–421

    Article  CAS  PubMed  Google Scholar 

  • Hopkins WG, Hüner NPA (2009) Introduction to plant physiology, 4th edn. Wiley, New York

    Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  CAS  PubMed  Google Scholar 

  • 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 275:1069–1079

    Article  CAS  PubMed  Google Scholar 

  • Hüner NPA, Grodzinski B (2011) Photosynthesis and photoautotrophy. In Moo-Young M (ed) Comprehensive Biotechnology, vol 1, 2nd edn. Elsevier, Amsterdam, pp 315-322

  • Hüner NPA, Elfman B, Krol M, MacIntosh A (1984) Growth and development at cold hardening temperatures. Chloroplast ultrastructure, pigment content and composition. Can J Bot 62:53–60

    Article  Google Scholar 

  • Hüner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hüner NPA, Öquist G, Melis A (2003) Photostasis in plants, green algae and cyanobacteria: the role of light harvesting antenna complexes. In: Green BR, Parson WW (eds) Advances in photosynthesis and respiration. Light harvesting antennas in photosynthesis, vol 13. Kluwer, Dordrecht, pp 401–421

    Chapter  Google Scholar 

  • Hüner NPA, Dahal K, Hollis L, Bode R, Rosso D, Krol M, Ivanov AG (2012) Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front Plant Physiol 3:Article 255

  • Hüner NPA, Bode R, Dahal K, Busch FA, Possmayer M, Szyszka B, Rosso D, Ensminger I, Krol M, Ivanov AG, Maxwell DP (2013) Shedding some light on cold acclimation, cold adaptation, and phenotypic plasticity. Botany 91:127–136

    Article  CAS  Google Scholar 

  • Hüner NPA, Dahal K, Kurepin LV, Savitch L, Singh J, Ivanov AG, Kane K, Sarhan F (2014) Potential for increased photosynthetic performance and crop productivity in response to climate change: role of CBFs and gibberellic acid. Front Chem 2:Artcle 18

  • Hussain A, Peng J (2003) Della proteins and GA signalling in Arabidopsis. J Plant Growth Regul 22:134–140

    Article  CAS  Google Scholar 

  • Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15. doi:10.1093/nar/gng015

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Hüner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Hendrickson L, Krol M, Selstam E, Öquist G, Hurry V, Hüner NPA (2006) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157

    Article  CAS  PubMed  Google Scholar 

  • Ivanov AG, Morgan-Kiss RM, Krol M, Allakhverdiev SI, Zanev Yu, Sane PV, Hüner NPA (2015) Photoinhibition of photosystem I in a pea mutant with altered LHCII organization. J Photochem Photobiol B 152:335–346

    Article  CAS  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  CAS  PubMed  Google Scholar 

  • Jahns P, Holzwarth AJ (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Ke B (2001) Photosynthesis. Photobiochemistry and photobiophysics. In: Advances in photosynthesis, vol 10. Kluwer, Dordrecht

  • Khandelwal A, Elvitigala T, Ghosh B, Quatrano RS (2008) Arabidopsis transcriptome reveals control circuits regulating redox homeostasis and the role of an AP2 transcription factor. Plant Physiol 148:2050–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim C, Apel K (2013) Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res 116:455–464

    Article  CAS  PubMed  Google Scholar 

  • Kindgren P, Noren L, Barajas Lopez J-D, Shaikhali J, Strand Å (2012) Interplay between heat shock protein 90 and HY5 controls PhANG expression in response to the GUN5 plastid signal. Mol Plant 5:901–913

    Article  CAS  PubMed  Google Scholar 

  • Koscy G, Tari I, Vankova R, Zechmann B, Gulyas Z, Poor P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77–91

    Article  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574

    Article  CAS  Google Scholar 

  • Krol M, Griffith M, Hüner NPA (1984) An appropriate physiological control for environmental temperature studies: comparative growth kinetics for winter rye. Can J Bot 62:1062–1068

    Article  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 

  • Kurepin L, Dahal K, Savitch L, Singh J, Bode R, Ivanov AG, Hurry V, Hüner NPA (2013) Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int J Mol Sci 14:12729–12763

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leonardos ED, Savitch LV, Hüner NPA, Öquist G, Grodzinski B (2003) Daily photosynthetic and C-export patterns in winter wheat leaves during cold stress and acclimation. Physiol Plant 117:521–531

    Article  CAS  PubMed  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. In: Chilling, freezing, and high temperature stresses, vol 1. Academic Press, New York

  • Li Z, Wakao S, Fischer JBB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    Article  CAS  PubMed  Google Scholar 

  • Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibtion of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • Machalek KM, Davison IR, Falkowski PG (1996) Thermal acclimation and photoacclimation of photosynthesis in the brown alga Laminaria saccharina. Plant Cell Environ 19:1005–1016

    Article  CAS  Google Scholar 

  • Maxwell DP, Falk S, Trick CG, Hüner NPA (1994) Growth at low temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol 105:535–543

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maxwell DP, Laudenbach DE, Hüner NPA (1995) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109:787–795

    CAS  PubMed  PubMed Central  Google Scholar 

  • Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Melis A (1998) Photostasis in Plants. In: Williams G, Thistle T (eds) Photostasis and related Phenomena. Plenum Press, New York, pp 207–220

    Chapter  Google Scholar 

  • Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo ? Trends Plant Sci 4:130–135

    Article  PubMed  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  PubMed  Google Scholar 

  • Miskiewicz E, Ivanov AG, Williams JP, Khan MU, Falk S, Hüner NPA (2000) Photosynthetic acclimation of the filamentous cyanobacterium, Plectonema boryanum UTEX 485, to temperature and light. Plant Cell Physiol 41:767–775

    Article  CAS  PubMed  Google Scholar 

  • Miskiewicz E, Ivanov AG, Hüner NPA (2002) Stoichiometry of the photosynthetic apparatus and phycobilisome structure of the cyanobacterium Plectonema boryanum UTEX 485 are regulated by both light and temperature. Plant Physiol 130:1414–1425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, van Breusegem F (2011) ROS signalling: the new wave? Trends Plant Sci 16:300–308

    Article  CAS  PubMed  Google Scholar 

  • Miura E, Kato Y, Matsushima R, Albrech V, Laalami S, Sakamoto W (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell 19:1313–1328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ndong C, Danyluk J, Hüner NPA, Sarhan F (2001) Survey of gene expression in winter rye during changes in either growth temperature, irradiance or excitation pressure. Plant Mol Biol 45:691–703

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparison of shade and sun plants. In: Bowyer JR, Baker NR (eds) Photoinhibition of photosynthesis—from molecular mechanisms to the field. Bios Scientific Publishers, Oxford UK, pp 1–24

    Google Scholar 

  • Patel D, Franklin KA (2009) Temperature-regulation of plant architecture. Plant Signal Behav 4:577–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628

    Article  CAS  PubMed  Google Scholar 

  • Peng J, Harberd NP (1997) Giberellin deficiency and response mutations suppress stem elongation phenotype of phytochrome-deficient mutants of Arabidopsis. Plant Physiol 113:1051–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  CAS  PubMed  Google Scholar 

  • Perez IB, Brown PJ (2014) The role of ROS signalling in cross-tolerance: from model to crop. Front Plant Physiol 5:article 754

  • 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  CAS  PubMed  Google Scholar 

  • Petrillo E, Godoy Herz MA, Fuchs A, Reifer D, Fuller J, Yanovsky MJ, Simpson C, Brown JWS, Barta A, Kalyna M, Kornblihtt AR (2014) A chloroplast retrograde signal regulates nuclear alternative splicing. Science 344:427–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Pocock T, Hurry V, Savitch LV, Hüner NPA (2001) Susceptibility to low-temperature photoinhibition and the acquisition of freezing tolerance in winter and spring wheat: the role of growth temperature and irradiance. Physiol Plant 113:499–506

    Article  CAS  Google Scholar 

  • Pogson BJ, Woo NS, Förster B, Small ID (2008) Plastid signalling to the nucleus and beyond. Trends Plant Sci 13:602–609

    Article  CAS  PubMed  Google Scholar 

  • Queval G, Foyer CH (2012) Redox regulation of photosynthetic gene expression. Philos Trans R Soc B 367:3475–3485

    Article  CAS  Google Scholar 

  • Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, Maxwell DP, Hüner NPA (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142:574–585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosso D, Bode R, Li W, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Hüner NPA (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 21:3473–3492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruckle ME, Burgoon Lyle D, Lawrence Lauren A, Sinkler CA, Larkin RM (2012) Plastids are major regulators of light signaling in Arabidopsis. Plant Physiol 159:366–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savitch LV, Gray GR, Hüner NPA (1997) Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201:18–26

    Article  CAS  Google Scholar 

  • Savitch LV, Barker-Astrom J, Ivanov AG, Hurry V, Oquist G, Huner NPA, Gardestrom P (2001) Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity which is associated with an increased reduction of the chloroplast stroma. Planta 217:295–301

    Article  CAS  Google Scholar 

  • Savitch LV, Leonardos ED, Krol M, Jansson S, Grodzinski B, Hüner NPA, Öquist G (2002) Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation. Plant Cell Environ 25:761–771

    Article  CAS  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 49–70

    Google Scholar 

  • Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584

    Article  CAS  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Stoher E, Dietz K-J (2008) The dynamic thiol-disulphide redox proteome of the Arabidopsis thaliana chloroplast as revealed by differential electrophoretic mobility. Physiol Plant 133:566–583

    Article  CAS  Google Scholar 

  • Strand A, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ 26:523–535

    Article  CAS  Google Scholar 

  • Sukenik A, Wyman KD, Bennett J, Falkowski PG (1987) A novel mechanism for regulating the excitation of photosystem II in a green alga. Nature 327:704–707

    Article  CAS  Google Scholar 

  • Terashima I, Noguchi K, Itohnemoto T, Park YM, Kubo A, Tanaka K (1998) The cause of PSI photoinhibition at low temperatures in leaves of Cucumis sativus, a chilling-sensitive plant. Physiol Plant 103:295–303

    Article  CAS  Google Scholar 

  • Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kriuger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verhoeven A (2014) Sustained energy dissipation in winter evergreens. New Phytol 201:57–65

    Article  Google Scholar 

  • Vogel MO, Moore M, König K, Pecher P, Alsharafa K, Lee J, Dietz K-J (2014) Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell 26:1151–1165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson KE, Hüner NPA (2000) The role of growth rate, redox-state of the plastoquinone pool and the trans-thylakoid Delta pH in photoacclimation of Chlorella vulgaris to growth irradiance and temperature. Planta 212:93–102

    Article  CAS  PubMed  Google Scholar 

  • Wilson KE, Krol M, Hüner NPA (2003) Temperature-induced greening of Chlorella vulgaris. The role of the cellular energy balance and zeaxanthin-dependent nonphotochemical quenching. Planta 217:616–627

    Article  CAS  PubMed  Google Scholar 

  • Wilson KE, Ivanov AG, Öquist G, Grodzinski B, Sarhan F, Hüner NPA (2006) Energy balance, organellar redox status and acclimation to environmental stress. Can J Bot 84:1355–1370

    Article  CAS  Google Scholar 

  • Wingler A (2015) Comparison of signalling interactions determining annual and perennial plant growth in response to low temperature. Front Plant Physiol 5:794–814

    Google Scholar 

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Yu F, Fu A, Aluru M, Park S, Xu Y, Liu H, Liu X, Foudree A, Nambogga M, Rodermel S (2007) Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ 30:350–365

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to David Carter at the London Regional Genomics Center (Robarts Research Institute, London, Ontario, Canada) for processing all the microarray chips and providing the license and training for the use of Partek. This research was supported by grants to NPAH from NSERC, CFI and the CRC programmes.

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  1. Rainer Bode

    Present address: Department of Biology, Chemistry and Pharmacy, Institute of Biology – Physiology of Plants, Freie Universität Berlin, Königin-Luise-Straße 12-16, 14195, Berlin, Germany

Authors and Affiliations

  1. Department of Biology and The Biotron Centre for Experimental Climate Change Research, Western University, London, ON, N6A 5B7, Canada

    Rainer Bode, Alexander G. Ivanov & Norman P. A. Hüner

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  1. Rainer Bode
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  2. Alexander G. Ivanov
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Correspondence to Norman P. A. Hüner.

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Bode, R., Ivanov, A.G. & Hüner, N.P.A. Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis . Photosynth Res 128, 287–312 (2016). https://doi.org/10.1007/s11120-016-0245-y

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