Rapid transcriptional and metabolic regulation of the deacclimation process in cold acclimated Arabidopsis thaliana

Springer Science and Business Media LLC - Tập 18 - Trang 1-17 - 2017
Majken Pagter1,2, Jessica Alpers1, Alexander Erban1, Joachim Kopka1, Ellen Zuther1, Dirk K. Hincha1
1Max-Planck-Institut für Molekulare Pflanzenphysiologie, Potsdam, Germany
2Present address: Chemistry and Bioscience, Aalborg University, Aalborg East, Denmark

Tóm tắt

During low temperature exposure, temperate plant species increase their freezing tolerance in a process termed cold acclimation. This is accompanied by dampened oscillations of circadian clock genes and disrupted oscillations of output genes and metabolites. During deacclimation in response to warm temperatures, cold acclimated plants lose freezing tolerance and resume growth and development. While considerable effort has been directed toward understanding the molecular and metabolic basis of cold acclimation, much less information is available about the regulation of deacclimation. We report metabolic (gas chromatography-mass spectrometry) and transcriptional (microarrays, quantitative RT-PCR) responses underlying deacclimation during the first 24 h after a shift of Arabidopsis thaliana (Columbia-0) plants cold acclimated at 4 °C back to warm temperature (20 °C). The data reveal a faster response of the transcriptome than of the metabolome and provide evidence for tightly regulated temporal responses at both levels. Metabolically, deacclimation is associated with decreasing contents of sugars, amino acids, glycolytic and TCA cycle intermediates, indicating an increased need for carbon sources and respiratory energy production for the activation of growth. The early phase of deacclimation also involves extensive down-regulation of protein synthesis and changes in the metabolism of lipids and cell wall components. Hormonal regulation appears particularly important during deacclimation, with extensive changes in the expression of genes related to auxin, gibberellin, brassinosteroid, jasmonate and ethylene metabolism. Members of several transcription factor families that control fundamental aspects of morphogenesis and development are significantly regulated during deacclimation, emphasizing that loss of freezing tolerance and growth resumption are transcriptionally highly interrelated processes. Expression patterns of some clock oscillator components resembled those under warm conditions, indicating at least partial re-activation of the circadian clock during deacclimation. This study provides the first combined metabolomic and transcriptomic analysis of the regulation of deacclimation in cold acclimated plants. The data indicate cascades of rapidly regulated genes and metabolites that underlie the developmental switch resulting in reduced freezing tolerance and the resumption of growth. They constitute a large-scale dataset of genes, metabolites and pathways that are crucial during the initial phase of deacclimation. The data will be an important reference for further analyses of this and other important but under-researched stress deacclimation processes.

Tài liệu tham khảo

Xin Z, Browse J. Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ. 2000;23:893–902. Guy CL, Kaplan F, Kopka J, Selbig J, Hincha DK. Metabolomics of temperature stress. Physiol Plant. 2008;132:220–35. Hincha DK, Espinoza C, Zuther E. Transcriptomic and metabolomic approaches to the analysis of plant freezing tolerance and cold acclimation. In: Tuteja N, Gill SS, Tiburcio AF, Tuteja R, editors. In: Improving Crop Resistance to Abiotic Stress, vol. 1. Berlin: Wiley-Blackwell; 2012. p. 255–87. Thomashow MF. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 2010;154:571–7. Chinnusamy V, Zhu J, Zhu J-K. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12:444–51. Shi Y, Ding Y, Yang S. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol. 2015;56:7–15. Kalberer SR, Wisniewski M, Arora R. Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Sci. 2006;171:3–16. Pagter M, Arora R. Winter survival and deacclimation of perennials under warmer climate: physiological perspectives. Physiol Plant. 2013;147:75–87. IPCC: Summary for policymakers. In: Climate Change 2013: The Physical Science Basis Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Edited by Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM. Cambridge, United Kingdom; New York, NY, USA: Cambridge University Press; 2013. Vitasse Y, Lenz A, Körner C. The interaction between freezing tolerance and phenology in temperate deciduous trees. Frontiers Plant Sci. 2014;5:541. Fitter AH, Fitter RSR. Rapid changes in flowering time in British plants. Science. 2002;296:1689–91. Karlsen SR, Solheim I, Beck PSA, Høgda KA, Wielgolaski FE, Tømmervik H. Variability of the start of the growing season in Fennoscandia. Int J Biometeorol. 2007;51:513–24. Jönsson AM, Baaring L. Ensemble analysis of frost damage on vegetation caused by spring backlashes in a warmer Europe. Nat Hazards Earth Syst Sci. 2011;11:401–18. Byun Y-J, Koo M-Y, Joo H-J, Ha-Lee Y-M, Lee D-H. Comparative analysis of gene expression under cold acclimation, deacclimation and reacclimation in Arabidopsis. Physiol Plant. 2014;152:256–74. Hoffman L, DaCosta M, Bertrand A, Castonguay Y, Ebdon JS. Comparative assessment of metabolic responses to cold acclimation and deacclimation in annual bluegrass and creeping bentgrass. Environ Exp Bot. 2014;106:197–206. Kalberer SR, Leyva-Estrada N, Krebs SL, Arora R. Frost dehardening and rehardening of floral buds of deciduous azaleas are influenced by genotypic biogeography. Environ Exp Bot. 2007;59:264–75. Zuther E, Juszczak I, Lee YP, Baier M, Hincha DK. Time-dependent deacclimation after cold acclimation in Arabidopsis thaliana accessions. Sci Rep. 2015;5:12199. Pagter M, Hausman J-F, Arora R. Deacclimation kinetics and carbohydrate changes in stem tissues of Hydrangea in response to an experimental warm spell. Plant Sci. 2011;180:140–8. Pagter M, Lefevre I, Arora R, Hausman J-F. Quantitative and qualitative changes in carbohydrates associated with spring deacclimation in contrasting Hydrangea species. Environ Exp Bot. 2011;72:358–67. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics. 2006;6:212–34. Juszczak I, Cvetkovic J, Zuther E, Hincha DK, Baier M. Natural variation of cold deacclimation correlates with variation of cold-acclimation of the plastid antioxidant system in Arabidopsis thaliana accessions. Front Plant Sci. 2016;7:305. Welling A, Palva ET. Involvement of CBF transcription factors in winter hardiness in birch. Plant Physiol. 2008;147:1199–211. Hannah MA, Heyer AG, Hincha DK. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet. 2005;1:e26. Rohde P, Hincha DK, Heyer AG. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J. 2004;38:790–9. Bieniawska Z, Espinoza C, Schlereth A, Sulpice R, Hincha DK, Hannah MA. Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol. 2008;147:263–79. Czechowski T, Bari R, Stitt M, Scheible W-R, Udvardi M. Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J. 2004;38:366–79. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible W-R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139:5–17. Zuther E, Schulz E, Childs LH, Hincha DK. Natural variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ. 2012;35:1860–78. Le MQ, Pagter M, Hincha DK. Global changes in gene expression, assayed by microarray hybridization and quantitative RT-PCR, during acclimation of three Arabidopsis thaliana accessions to sub-zero temperatures after cold acclimation. Plant Mol Biol. 2015;87:1–15. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B. 1995;57:289–300. Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucl Acids Res. 2012;40:W622–7. Dethloff F, Erban A, Orf I, Alpers J, Fehrle I, Beine-Golovchuk O, Schmidt S, Schwachtje J, Kopka J. Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry. In: Hincha DK, Zuther E, editors. In: Plant Cold Acclimation, vol. 1166. New York: Springer; 2014. p. 171–98. Li X, Lawas LMF, Malo R, Glaubitz U, Erban A, Mauleon R, Heuer S, Zuther E, Kopka J, Hincha DK, et al. Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant Cell Environ. 2015;38:2171–92. Golm Metabolome Database. http://gmd.mpimp-golm.mpg.de/. Stacklies W, Redestig H, Scholz M, Walther D, Selbig J. pcaMethods: a bioconductor package providing PCA methods for incomplete data. Bioinformatics. 2007;23:1164–7. Usadel B, Nagel A, Steinhauser D, Gibon Y, Bläsing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, et al. PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinf. 2006;7:535. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. TM4: A free, open-source system for microarray data management and analysis. BioTechniques. 2003;34:374–8. Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA. The interaction between diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS One. 2010;5:e14101. Bläsing OE, Gibon Y, Günther M, Höhne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell. 2005;17:3257–81. Medina J, Catala R, Salinas J. The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci. 2011;180:3–11. Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu J-K. Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiol. 2016;171:2744–59. Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant. 2010;3:224–35. Winter H, Huber SC. Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Critical Rev Biochem Mol Biol. 2000;35:253–89. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL. Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol. 2004;136:4159–68. Gibbs DJ, Conde JV, Berkhan S, Prasad G, Mendiondo GM, Holdsworth MJ. Group VII ethylene response factors coordinate oxygen and nitric oxide signal transduction and stress responses in plants. Plant Physiol. 2015;169:23–31. Pagter M, Sergeant K, Møller SM, Bertram HC, Renaut J. Changes in the proteome and water state in bark and xylem of Hydrangea paniculata during loss of freezing tolerance. Environ Exp Bot. 2014;106:99–111. Michaeli S, Fromm H. Closing the loop on the GABA shunt in plants: are GABA metabolism and signaling entwined? Front Plant Sci. 2015;6:419. Mazzucotelli E, Tartari A, Cattivelli L, Forlani G. Metabolism of gamma-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot. 2006;57:3755–66. Zeier J. New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ. 2013;36:2085–103. Degenkolbe T, Giavalisco P, Zuther E, Seiwert B, Hincha DK, Willmitzer L. Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. Plant J. 2012;72:972–82. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol. 2006;142:98–112. Korn M, Peterek S, Mock H-P, Heyer AG, Hincha DK. Heterosis in the freezing tolerance, and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ. 2008;31:813–27. Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK. Natural variation in flavonol and anthocyanin metabolism during cold acclimation in Arabidopsis thaliana accessions. Plant Cell Environ. 2015;38:1658–72. Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK. Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana. Sci Rep. 2016;6:34027. Fragkostefanakis S, Röth S, Schleiff E, Scharf K-D. Prospects of engineering thermotolerance in crops through modulation of heat stress transcription factor and heat shock protein networks. Plant Cell Environ. 2015;38:1881–95. Liu H-C, Charng Y-Y. Common and distinct functions of Arabidopsis class A1and A2 heat shock factors in diverse abiotic stress responses and development. Plant Physiol. 2013;163:276–90. Prasch CM, Sonnewald U. Signaling events in plants: stress factors in combination change the picture. Environ Exp Bot. 2015;114:4–14. Colebrook EH, Thomas SG, Phillips AL, Hedden P. The role of gibberellin signalling in plant responses to abiotic stress. J Exp Bot. 2014;217:67–75. Liscum E, Reed JW. Genetics of aux/IAA and ARF action in plant growth and development. Plant Mol Biol. 2002;49:387–400. Raschke A, Ibañez C, Ullrich KK, Anwer MU, Becker S, Glöckner A, Trenner J, Denk K, Saal B, Sun X, et al. Natural variation of ELF3 affects thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes. BMC Plant Biol. 2015;15:197. Proveniers MCG, van Zanten M. High temperature acclimation through PIF4 signaling. Trends Plant Sci. 2013;18:59–64. Sun J, Qi L, Li Y, Zhai Q, Li C. PIF4 And PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell. 2013;25:2102–14. Ren H, Gray WM. SAUR proteins as effectors of hormonal and environmental signals in plant growth. Mol Plant. 2015;8:1153–64. Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot. 2005;95:707–35. Kurepin LV, Dahal KP, Savitch LV, Singh J, Bode R, Ivanov AG, Hurry V, Hüner NPA. Role of CBFs as integrators of chloroplast redox, phytochrome and plant hormone signaling during cold acclimation. Int J Mol Sci. 2013;14:12729–63. Davière J-M, Achard P. A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant. 2016;9:10–20. Li J, Nagpal P, Vitart V, McMorris TC, Chory J. A role for brassinosteroids in light-dependent development of Arabidopsis. Nature. 1996;272:398–401. Kazan K. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 2015;20:163–71. Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K. Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol. 2013;163:291–304. Rodrigues MA, Bianchetti RE, Freschi L. Shedding light on ethylene metabolism in higher plants. Front Plant Sci. 2014;5:665. Yruela I. Plant development regulation: overview and perspectives. J Plant Physiol. 2015;182:62–78. Ariel FD, Manavella PA, Dezar CA, Chan RL. The true story of the HD-zip family. Trends Plant Sci. 2007;12:419–26. Tan Q, Irish VF. The Arabidopsis zinc finger-homeodomain genes encode proteins with unique biochemical properties that are coordinately expressed during floral development. Plant Physiol. 2006;140:1095–108. Gangappa SN, Botto JF. The BBX family of plant transcription factors. Trends Plant Sci. 2014;19:460–70. Feller A, Machemer K, Braun EL, Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 2011;66:94–116. Leivar P, Quail PH. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 2011;16:19–28. Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmestad RG, Imaizumi T. FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109:3582–7. Nagel DH, Pruneda-Paz JL, Kay SA. FBH1 Affects warm temperature responses in the Arabidopsis circadian clock. Proc Natl Acad Sci U S A. 2014;111:14595–600. Schuster C, Gaillochet C, Medzihradszky A, Busch W, Daum G, Krebs M, Kehle A, Lohmann JU. A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals. Dev Cell. 2014;28:438–49. Bas R, Bao DP, van Eck-Stouten E, Brand M, Smeekens S, Proveniers M. Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J. 2009;58:641–54. Papuga J, Hoffmann C, Dieterle M, Moes M, Moreau F, Tholl S, Steinmetz A, Thomas C. Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation. Plant Cell. 2010;22:3034–52. Aguilar-Martínez A, Sinha N. Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development. Frontiers Plant Sci. 2013;4:406. Kumimoto RW, Zhang Y, Siefers N, Holt BF. NF-YC3, NF-YC4 and NF-YC9 are required for CONSTANS-mediated, photoperiod-dependent flowering in Arabidopsis thaliana. Plant J. 2010;63:379–91. Fogelmark K, Troein C. Rethinking transcriptional activation in the Arabidopsis circadian clock. PLoS Comp Biol. 2014;10:e1003705. Kuno N, Møller SG, Shinomura T, Xu XM, Chua N-H, Furuya M. The novel MYB protein EARLY-PHYTOCHROME-RESPONSIVE1 is a component of a slave circadian oscillator in Arabidopsis. Plant Cell. 2003;15:2476–88. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL. REVEILLE1, A Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci U S A. 2009;106:16883–8. Meissner M, Orsini E, Ruschhaupt M, Melchinger AE, Hincha DK, Heyer AG. Mapping quantitative trait loci for freezing tolerance in a recombinant inbred line population of Arabidopsis thaliana accessions Tenela and C24 reveals REVEILLE1 as negative regulator of cold acclimation. Plant Cell Environ. 2013;36:1256–67.