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The up-regulation of elongation factors in the barley leaf and the down-regulation of nucleosome assembly genes in the crown are both associated with the expression of frost tolerance

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Abstract

We report a series of microarray-based leaf and crown transcriptome comparisons involving three barley cultivars (cvs. Luxor, Igri and Atlas 68) which express differing degrees of frost tolerance. The transcripts were obtained following the exposure of seedlings to low (above and below zero) temperatures, aiming to identify those genes and signalling/metabolic pathways which are associated with frost tolerance. Both the leaves and the crowns responded to low temperature by the up-regulation of a suite of abscisic acid (ABA)-responsive genes, most of which have already been recognized as components of the plant low temperature response. The inter-cultivar comparison indicated that genes involved in maintaining the leaf's capacity to synthesize protein and to retain chloroplast activity were important for the expression of frost tolerance. In the crown, the repression of genes associated with nucleosome assembly and transposon regulation were the most relevant transcriptional changes associated with frost tolerance, highlighting the role of gene repression in the cold acclimation response.

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References

  • Begcy K, Mariano ED, Mattiello L, Nunes AV, Mazzafera P, Maia IG, Menossi M (2011) An Arabidopsis mitochondrial uncoupling protein confers tolerance to drought and salt stress in transgenic tobacco plants. PLoS ONE 6:e23776. doi:10.1371/journal.pone.0023776

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Campoli C, Matus-Cádiz MA, Pozniak CJ, Cattivelli L, Fowler DB (2009) Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol Genet Genomics 282:141–152

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chi WT, Fung RW, Liu HC, Hsu CC, Charng YY (2009) Temperature-induced lipocalin is required for basal and acquired thermotolerance in Arabidopsis. Plant Cell Environ 32:917–927. doi:10.1111/j.1365-3040.2009.01972.x

    Article  CAS  PubMed  Google Scholar 

  • Chu B, Snustad DP, Carter JV (1993) Alteration of beta-tubulin gene expression during low-temperature exposure in leaves of Arabidopsis thaliana. Plant Physiol 103:371–377

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chung S, Parish RW (2008) Combinatorial interactions of multiple cis-elements regulating the induction of the Arabidopsis XERO2 dehydrin gene by abscisic acid and cold. Plant J 54:15–29

    Article  CAS  PubMed  Google Scholar 

  • Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22 K Barley GeneChip comes of age. Plant Physiol 134:960–968

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szuecs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genomics 10:582. doi:10.1186/1471-2164-10-582

    Article  PubMed Central  PubMed  Google Scholar 

  • Dinari A, Niazi A, Afsharifar AR, Ramezani A (2013) Identification of upregulated genes under cold stress in cold-tolerant chickpea using the cDNA-AFLP approach. PLoS ONE 8:e52757. doi:10.1371/journal.pone.0052757

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Doyle EA, Lane AM, Sides JM, Mudgett MB, Monroe JD (2007) An alpha-amylase (At4g25000) in Arabidopsis leaves is secreted and induced by biotic and abiotic stress. Plant Cell Environ 30:388–398

    Article  CAS  PubMed  Google Scholar 

  • Fisk SP, Cuesta-Marcos A, Cistué L, Russell J, Smith KP, Baenziger S, Bedo Z, Corey A, Filichkin T, Karsai I, Waugh R, Hayes PM (2013) FR-H3: a new QTL to assist in the development of fall-sown barley with superior low temperature tolerance. Theor Appl Genet 126:335–347. doi:10.1007/s00122-012-1982-8

    Article  PubMed  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Francia E, Barabaschi D, Tondelli A, Laidò G, Rizza F, Stanca AM, Busconi M, Fogher C, Stockinger EJ, Pecchioni N (2007) Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091

    Article  CAS  PubMed  Google Scholar 

  • Funck D, Eckard S, Mueller G (2010) Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. BMC Plant Biol 10:70

    Article  PubMed Central  PubMed  Google Scholar 

  • Gibson S, Arondel V, Iba K, Somerville C (1994) Cloning of a temperature-regulated gene encoding a chloroplast ω-3 desaturase from Arabidopsis thaliana. Plant Physiol 106:1615–1621. doi:10.1104/pp. 106.4.1615

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157. doi:10.1042/BJ20041931

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gray GR, Chauvin LP, Sarhan F, Huner NPA (1997) Cold acclimation and freezing tolerance—a complex interaction of light and temperature. Plant Physiol 114:467–474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Griffith M, Yaish MWF (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  CAS  PubMed  Google Scholar 

  • Griffith M, Lumb C, Ala P, Yang DSC, Hon W-C, Moffatt BA (1992) Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol 100:593–596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo Y, Xiong L, Ishitani M, Zhu JK (2002) An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc Natl Acad Sci U S A 99:7786–7791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767. doi:10.1093/jxb/ert040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Article  CAS  Google Scholar 

  • Hashida SN, Uchiyama T, Martin C, Kishima Y, Sano Y, Mikami T (2006) The temperature-dependent change in methylation of the Antirrhinum transposon Tam3 is controlled by the activity of its transposase. Plant Cell 18:104–118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Herman EM, Rotter K, Premakumar R, Elwinger G, Bae R, Ehler-King L, Chen S, Livingston DP III (2006) Additional freeze hardiness in wheat acquired by exposure to −3°C is associated with extensive physiological, morphological, and molecular changes. J Exp Bot 57:3601–3618

    Article  CAS  PubMed  Google Scholar 

  • Hillwig M, Lebrasseur N, Green P, Macintosh G (2008) Impact of transcriptional, ABA-dependent, and ABA-independent pathways on wounding regulation of RNS1 expression. Mol Genet Genomics 280:249–261. doi:10.1007/s00438-008-0360-3

    CAS  PubMed  Google Scholar 

  • Houde M, Dhindsa RS, Sarhan F (1992) A molecular marker to select for freezing tolerance in Gramineae. Mol Genet Genomics 234:43–48

    CAS  Google Scholar 

  • Ihaka R, Gentleman R (1996) A language for data analysis and graphics. J Comput Graph Stat 5:299–314. doi:10.2307/1390807

    Google Scholar 

  • Irizarry RA, Gautier L, Bolstad BM, Miller C with contributions from Astrand M, Cope LM, Gentleman R, Gentry J, Halling C, Huber W, MacDonald J, Rubinstein BIP, Workman C, Zhang J (2006) Affy: methods for Affymetrix oligonucleotide arrays. R package version 1.12.1

  • Janáček J, Prášil I (1991) Quantification of plant frost injury by nonlinear fitting of an S-shaped function. Cryog Lett 12:47–52

    Google Scholar 

  • Janská A, Aprile A, Zámečník J, Cattivelli L, Ovesná J (2011) Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct Integr Genomics 11:307–325. doi:10.1007/s10142-011-0213-8

    Article  PubMed Central  PubMed  Google Scholar 

  • Janská A, Hodek J, Svoboda P, Zámečník J, Prášil IT, Vlasáková E, Milella L, Ovesná J (2013) The choice of reference gene set for assessing gene expression in barley (Hordeum vulgare L.) under low temperature and drought stress. Mol Genet Genomics 288:639–649. doi:10.1007/s00438-013-0774-4

    PubMed  Google Scholar 

  • Kandasamy MK, Gilliland LU, McKinney EC, Meagher RB (2001) One plant actin isovariant, act7, is induced by auxin and required for normal callus formation. Plant Cell 13:1541–1554

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci U S A 107:15986–15991

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kocsy G, Athmer B, Perovic D, Himmelbach A, Szűcs A, Vashegyi I, Schweizer P, Galiba G, Stein N (2010) Regulation of gene expression by chromosome 5A during cold hardening in wheat. Mol Genet Genomics 283:351–363

    CAS  PubMed  Google Scholar 

  • Kodama H, Horiguchi G, Nishiuchi T, Nishimura M, Iba K (1995) Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves. Plant Physiol 107:1177–1185

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kohonen T, Hynninen J, Kangas J, Laaksonen J (1996) SOM-PAK, the self-organizing map program package (version 3.1). http://www.cis.hut.fi/research/papers/som\_tr96.ps.Z

  • Kosová K, Holková L, Prášil IT, Prášilová P, Bradáčová M, Vítámvás P, Čapková V (2008) Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare). J Plant Physiol 165:1142–1151

    Article  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Prášilová P, Prášil IT (2013) Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale. Biol Plant 57:105–112. doi:10.1007/s10535-012-0237-5

    Article  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147

    Article  CAS  PubMed  Google Scholar 

  • Latijnhouwers M, Xu XM, Møller SG (2010) Arabidopsis stromal 70-kDa heat shock proteins are essential for chloroplast development. Planta 232:567–578. doi:10.1007/s00425-010-1192-z

    Article  CAS  PubMed  Google Scholar 

  • Latz A, Mehlmer N, Zapf S, Mueller TD, Wurzinger B, Pfister B, Csaszar E, Hedrich R, Teige M, Becker D (2012) Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium dependent protein kinases (CDPKs). Mol Plant. doi:10.1093/mp/sss158

    PubMed Central  PubMed  Google Scholar 

  • Lee Y, Choi D, Kende H (2001) Expansins: ever-expanding numbers and functions. Curr Opin Plant Biol 4:527

    Article  CAS  PubMed  Google Scholar 

  • Leshem Y, Golani Y, Kaye Y, Levine A (2010) Reduced expression of the v-SNAREs AtVAMP71/AtVAMP7C gene family in Arabidopsis reduces drought tolerance by suppression of abscisic acid-dependent stomatal closure. J Exp Bot 61:2615–2622. doi:10.1093/jxb/erq099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lev S (2012) Nonvesicular lipid transfer from the endoplasmic reticulum. Cold Spring Harb Perspect Biol 4:a013300. doi:10.1101/cshperspect.a013300

    Article  PubMed  Google Scholar 

  • Livingston DP III, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol 116:403–408

    Article  CAS  PubMed Central  Google Scholar 

  • Livingston DP III, Van K, Premakumar R, Tallury SP, Herman EM (2007) Using Arabidopsis thaliana as a model to study subzero acclimation in small grains. Cryobiology 54:154–163

    Article  CAS  PubMed  Google Scholar 

  • McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, van der Does D, Laurière C, Munnik T, Haring MA, Testerink C (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J 72:436–449. doi:10.1111/j.1365-313X.2012.05089.x

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Medina J, Ballesteros ML, Salinas J (2007) Phylogenetic and functional analysis of Arabidopsis RCI2 genes. J Exp Bot 58:4333–4346

    Article  CAS  PubMed  Google Scholar 

  • Moreno AA, Orellana A (2011) The physiological role of the unfolded protein response in plants. Biol Res 44:75–80

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose as a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263. doi:10.1104/pp.108.122465

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci U S A 101:3985–3990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Olien CR (1967) Freezing stress and survival. Ann Rev Plant Physiol 18:387–408

    Article  Google Scholar 

  • Perras M, Sarhan F (1989) Synthesis of freezing tolerance proteins in leaves, crown, and roots during cold acclimation of wheat. Plant Physiol 89:577–585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips MA, León P, Boronat A, Rodríguez-Concepción M (2008) The plastidial MEP pathway: unified nomenclature and resources. Trends Plant Sci 13:619–623. doi:10.1016/j.tplants.2008.09.003

    Article  CAS  PubMed  Google Scholar 

  • Pillot M, Autran D, Leblanc O, Grimanelli D (2010) A role for CHROMOMETHYLASE3 in mediating transposon and euchromatin silencing during egg cell reprogramming in Arabidopsis. Plant Signal Behav 5:1167–1170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Prášil I, Zámečník J (1998) The use of a conductivity measurement method for assessing freezing injury. I. Influence of leakage time, segment number, size and shape in a sample on evaluation of the degree of injury. Environ Exp Bot 40:1–10

    Article  Google Scholar 

  • Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci U S A 96:15354–15361. doi:10.1073/pnas.96.26.15354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Quesada V, Sarmiento-Mañús R, González-Bayón R, Hricová A, Ponce MR, Micol JL (2013) Porphobilinogen deaminase deficiency alters vegetative and reproductive development and causes lesions in Arabidopsis. PLoS ONE 8:e53378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez-Franco M, Sarmiento F, Marquardt K, Markus R, Neuhaus G (2008) Does light taste salty? Plant Signal Behav 3:72–73

    Article  PubMed Central  PubMed  Google Scholar 

  • Ruel K, Berrio-Sierra J, Derikvand MM, Pollet B, Thévenin J, Lapierre C, Jouanin L, Joseleau JP (2009) Impact of CCR1 silencing on the assembly of lignified secondary walls in Arabidopsis thaliana. New Phytol 184:99–113. doi:10.1111/j.1469-8137.2009.02951.x

    Article  CAS  PubMed  Google Scholar 

  • Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Guldener U, Mannhaupt G, Munsterkotter M, Mewes HW (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res 32:5539–5545

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ruppel N, Hangarter R (2007) Mutations in a plastid-localized elongation factor G alter early stages of plastid development in Arabidopsis thaliana. BMC Plant Biol 7:37

    Article  PubMed Central  PubMed  Google Scholar 

  • Samol I, Rossig C, Buhr F, Springer A, Pollmann S, Lahroussi A, von Wettstein D, Reinbothe C, Reinbothe S (2011) The outer chloroplast envelope protein OEP16-1 for plastid import of NADPH: protochlorophyllide oxidoreductase A in Arabidopsis thaliana. Plant Cell Physiol 52:96–111. doi:10.1093/pcp/pcq177

    CAS  PubMed  Google Scholar 

  • Sangwan V, Örvar BL, Dhindsa RS (2002) Early events during low temperature signaling. In: Li C, Palva ET (eds) Plant cold hardiness. Kluwer Academic Publishers, Dordrecht, pp 43–53

    Chapter  Google Scholar 

  • Shen Q, Chen CN, Brands A, Pan SM, Ho TH (2001) The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Mol Biol 45:327–340

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular response to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    Article  CAS  PubMed  Google Scholar 

  • Skinner DZ (2009) Post-acclimation transcriptome adjustment is a major factor in freezing tolerance of winter wheat. Funct Integr Genomics 9:513–523

    Article  CAS  PubMed  Google Scholar 

  • Skinner JS, Von Zitzewitz J, Szűcs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551

    Article  CAS  PubMed  Google Scholar 

  • Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mo B 3: Article 3

  • Song JT, Lu H, Greenberg JT (2004) Divergent roles in Arabidopsis thaliana development and defense of two homologous genes, ABERRANT GROWTH AND DEATH2 and AGD2-LIKE DEFENSE RESPONSE PROTEIN1, encoding novel aminotransferases. Plant Cell 16:353–366. doi:10.1105/tpc.019372

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sutton F, Chen DG, Ge X, Kenefick D (2009) Cbf genes of the Fr-A2 allele are differentially regulated between long-term cold acclimated crown tissue of freeze-resistant and -susceptible, winter wheat mutant lines. BMC Plant Biol 9:34

    Article  PubMed Central  PubMed  Google Scholar 

  • Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, Cattivelli L (2006) Transcriptome analysis of cold acclimation in barley Albina and Xantha mutants. Plant Physiol 141:257–270

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sweetlove LJ, Lytovchenko A, Morgan M, Nunes-Nesi A, Taylor NL, Baxter CJ, Eickmeier I, Fernie AR (2006) Mitochondrial uncoupling protein is required for efficient photosynthesis. Proc Natl Acad Sci U S A 103:19587–19592

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28

    Article  PubMed  Google Scholar 

  • Talanova VV, Titov AF, Topchieva LV, Malysheva IE, Venzhik YV, Frolova SA (2009) Expression of WRKY transcription factor and stress protein genes in wheat plants during cold hardening and ABA treatment. Russ J Plant Physiol 56:702–708

    CAS  Google Scholar 

  • Tang W, Page M (2013) Transcription factor AtbZIP60 regulates expression of Ca2+-dependent protein kinase genes in transgenic cells. Mol Biol Rep 40:2723–2732

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol 50:571–599

    CAS  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411

    Article  CAS  PubMed  Google Scholar 

  • Tommasini L, Svensson JT, Rodriguez EM, Wahid A, Malatrasi M, Kato K, Wanamaker S, Resnik J, Close TJ (2008) Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct Integr Genomics 8:387–405

    Article  CAS  PubMed  Google Scholar 

  • Trunova TI (1965) Light and temperature systems in the hardening of winter wheat and the significance of oligosaccharides for frost resistance. Russ Plant Physiol 12:70–77

    Google Scholar 

  • Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89

    Article  CAS  Google Scholar 

  • Usadel B, Schluter U, Molhoj M, Gipmans M, Verma R, Kossmann J, Reiter WD, Pauly M (2004) Identification and characterization of a UDP-D-glucuronate 4-epimerase in Arabidopsis. FEBS Lett 569:327–331

    Article  CAS  PubMed  Google Scholar 

  • Van Buskirk HA, Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72–80

    Article  Google Scholar 

  • Vaultier M-N, Cantrel C, Vergnolle C, Justin A-M, Demandre C, Benhassaine-Kesri G, Cicek D, Zachowski A, Ruelland E (2006) Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Lett 580:4218–4223

    Article  CAS  PubMed  Google Scholar 

  • Vergnolle C, Vaultier M-N, Taconnat L, Renou J-P, Kader J-C, Zachowski A, Ruelland E (2005) The cold-induced early activation of phospholipase C and D pathways determines the response of two distinct clusters of genes in Arabidopsis cell suspensions. Plant Physiol 139:1217–1233. doi:10.1104/pp. 105.068171

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Li W, Li M, Welti R (2006) Profiling lipid changes in plant response to low temperatures. Physiol Plant 126:90–96

    Article  CAS  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Robertson AJ, Zheng P, Liu X, Gusta LV (2005) Identification and immunogold localization of a novel bromegrass (Bromus inermis Leyss) peroxisome channel protein induced by ABA, cold and drought stresses, and late embryogenesis. Gene 363:77–84

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183. doi:10.1105/tpc.000596

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu D, Huang X, Xu ZQ, Schläppi M (2011) The HyPRP gene EARLI1 has an auxiliary role for germinability and early seedling development under low temperature and salt stress conditions in Arabidopsis thaliana. Planta 234:565–577. doi:10.1007/s00425-011-1425-9

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16:599–608

    Article  PubMed  Google Scholar 

  • Zhang Y, Schläppi M (2007) Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta 227:233–243. doi:10.1007/s00425-007-0611-2

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Li X, He Z, Zhao X, Wang Q, Zhou B, Yu D, Huang X, Tang D, Guo X, Liu X (2013) Molecular character of a phosphatase 2C (PP2C) gene relation to stress tolerance in Arabidopsis thaliana. Mol Biol Rep 40:2633–2644

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This research was funded by the Czech Republic National Agency for Agricultural Research (project no. QH 81287), by the Czech Ministry of Agriculture (project no. Mze0002700604), by the Ministry of Education, Youth and Sports (project no. OC09032) and by the Italian Ministry of Agriculture, Special Project ESPLORA.

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Correspondence to Anna Janská.

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Supplementary Fig. 1

Hybridization quality. The plots show the mean intensity of each probe across a specific probe set, ordered from the 5′ to the 3′ end. All curves have a similar slope, implying that the hybridization quality was uniformly high. (GIF 408 kb)

High resolution image (TIFF 3,863 kb)

Supplementary Table 1

A complete list of genes differentially transcribed in (a) the leaf and (b) the crown. The genes have been classified into Lists/Groups and Clusters according to Fig. 3 (leaf) and Fig. 6 (crown). (1A 26,243 kb)

(1B 25,613 kb)

Supplementary Table 2

Genes transcribed in (a) the leaf and (b) the crown which map to regions harboring known QTL for frost tolerance (Fisk et al. 2013). Six regions were targeted: (1, 2) chromosome 1H 0–7 cM and 35–55 cM (the latter interval is the site of Fr-H3); (3) chromosome 4H 120–140 cM; (4, 5) chromosome 5H 85–110 cM (site of Fr-H2) and 129–154 cM (site of both Vrn-H1 and Fr-H1); and (6) chromosome 7H 132–142 cM. Transcription signal derived from microarray analysis. The classification of the genes according to list/group and cluster is given in Figs. 3 (leaf) and 6 (crown). (XLS 27,870 kb)

(XLS 27,239 kb)

Supplementary Table 3

Genes differentially transcribed (DTGs) in (a) the leaf and (b) the crown which map to regions harboring known QTL for frost tolerance (Fisk et al. 2013). Six regions were targeted: (1, 2) chromosome 1H 0–7 cM and 35–55 cM (the latter interval is the site of Fr-H3); (3) chromosome 4H 120–140 cM; (4, 5) chromosome 5H 85–110 cM (site of Fr-H2) and 129–154 cM (site of both Vrn-H1 and Fr-H1); and (6) chromosome 7H 132–142 cM. Transcript abundance derived from microarray analysis. The classification of the genes according to list/group and cluster is given in Figs. 3 (leaf) and 6 (crown). (DOC 219 kb)

(DOC 85 kb)

Supplementary Table 4

Genes differentially transcribed (DTGs) in (a) the leaf and (b) the crown which belong to a particular list/group and cluster, and which map to regions harboring known QTL for frost tolerance (Fisk et al. 2013). The DTGs referred to in the text are marked in bold. Six regions were targeted: (1, 2) chromosome 1H 0–7 cM and 35–55 cM (the latter interval is the site of Fr-H3); (3) chromosome 4H 120–140 cM; (4, 5) chromosome 5H 85–110 cM (site of Fr-H2) and 129–154 cM (site of both Vrn-H1 and Fr-H1); and (6) chromosome 7H 132–142 cM. Transcript abundance derived from microarray analysis. The classification of the genes according to list/group and cluster is given in Figs. 3 (leaf) and 6 (crown). (DOC 118 kb)

(DOC 45 kb)

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Janská, A., Aprile, A., Cattivelli, L. et al. The up-regulation of elongation factors in the barley leaf and the down-regulation of nucleosome assembly genes in the crown are both associated with the expression of frost tolerance. Funct Integr Genomics 14, 493–506 (2014). https://doi.org/10.1007/s10142-014-0377-0

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  • DOI: https://doi.org/10.1007/s10142-014-0377-0

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