Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
21360135
PubMed Central
PMC3098344
DOI
10.1007/s10142-011-0213-8
Knihovny.cz E-zdroje
- MeSH
- aklimatizace genetika MeSH
- GABA genetika metabolismus MeSH
- genetická transkripce MeSH
- histony genetika MeSH
- ječmen (rod) genetika metabolismus MeSH
- lignin biosyntéza genetika MeSH
- listy rostlin genetika metabolismus MeSH
- metabolismus sacharidů genetika MeSH
- nízká teplota * MeSH
- nukleozomy metabolismus MeSH
- proteiny teplotního šoku genetika MeSH
- regulace genové exprese u rostlin * MeSH
- roční období MeSH
- stanovení celkové genové exprese MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- GABA MeSH
- histony MeSH
- lignin MeSH
- nukleozomy MeSH
- proteiny teplotního šoku MeSH
We report a series of microarray-based comparisons of gene expression in the leaf and crown of the winter barley cultivar Luxor, following the exposure of young plants to various periods of low (above and below zero) temperatures. A transcriptomic analysis identified genes which were either expressed in both the leaf and crown, or specifically in one or the other. Among the former were genes responsible for calcium and abscisic acid signalling, polyamine synthesis, late embryogenesis abundant proteins and dehydrins. In the crown, the key organ for cereal overwintering, cold treatment induced transient changes in the transcription of nucleosome assembly genes, and especially H2A and HTA11, which have been implicated in cold sensing in Arabidopsis thaliana. In the leaf, various heat-shock proteins were induced. Differences in expression pattern between the crown and leaf were frequent for genes involved in certain pathways responsible for osmolyte production (sucrose and starch, raffinose, γ-aminobutyric acid metabolism), sugar signalling (trehalose metabolism) and secondary metabolism (lignin synthesis). The action of proteins with antifreeze activity, which were markedly induced during hardening, was demonstrated by a depression in the ice nucleation temperature.
Zobrazit více v PubMed
Atienza SG, Faccioli P, Perrotta G, Dalfino G, Zschiesche W, Humbeck K, Stanca AM, Cattivelli L. Large-scale analysis of transcript abundance in barley subjected to several single and combined abiotic stress conditions. Plant Sci. 2004;167:1359–1365. doi: 10.1016/j.plantsci.2004.07.006. DOI
Badawi M, Danyluk J, Boucho B, Houde M, Sarhan F. The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol Genet Genomics. 2007;277:533–554. doi: 10.1007/s00438-006-0206-9. PubMed DOI PMC
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57:289–300.
Brady SM, Sarkar SF, Bonetta D, McCourt P. The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signalling and lateral root development in Arabidopsis. Plant J. 2003;34:67–75. doi: 10.1046/j.1365-313X.2003.01707.x. PubMed DOI
Campoli C, Matus-Cádiz MA, Pozniak CJ, Cattivelli L, Fowler DB. Comparative expression of Cbf genes in the Triticeae under different acclimation induction temperatures. Mol Genet Genomics. 2009;282:141–152. doi: 10.1007/s00438-009-0451-9. PubMed DOI PMC
Cattivelli L, Baldi P, Crosatti C, Di Fonzo N, Faccioli P, Grossi M, Mastrangelo AM, Pecchioni N, Stanca AM. Chromosome regions and stress-related sequences involved in resistance to abiotic stress in Triticeae. Plant Mol Biol. 2002;48:649–665. doi: 10.1023/A:1014824404623. PubMed DOI
Century K, Reuber TL, Ratcliffe OJ. Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol. 2008;147:20–29. doi: 10.1104/pp.108.117887. PubMed DOI PMC
Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP. A new resource for cereal genomics: 22 K Barley GeneChip comes of age. Plant Physiol. 2004;134:960–968. doi: 10.1104/pp.103.034462. PubMed DOI PMC
Cuevas JC, Lopez-Cobollo R, Alcazar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A. Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating ABA levels in response to low temperature. Plant Physiol. 2008;148:1094–1105. doi: 10.1104/pp.108.122945. PubMed DOI PMC
D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J. Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J. 2006;48:857–872. doi: 10.1111/j.1365-313X.2006.02921.x. PubMed DOI
Dixon RA, Paiva NL. Stress-induced phenylpropanoid metabolism. Plant Cell. 1995;7:1085–1097. doi: 10.1105/tpc.7.7.1085. PubMed DOI PMC
Fowler DB. Cold acclimation threshold induction temperatures in cereals. Crop Sci. 2008;48:1147–1154. doi: 10.2135/cropsci2007.10.0581. DOI
Fowler S, Thomashow MF. Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell. 2002;14:1675–1690. doi: 10.1105/tpc.003483. PubMed DOI PMC
Franks F. Biophysics and biochemistry at low temperatures. Cambridge: Cambridge University Press; 1985.
Ganeshan S, Vitamvas P, Fowler DB, Chibbar RN. Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen. J Exp Bot. 2008;59:2393–2402. doi: 10.1093/jxb/ern112. PubMed DOI PMC
Gilmour SJ, Fowler SG, Thomashow MF. Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol. 2004;54:767–781. doi: 10.1023/B:PLAN.0000040902.06881.d4. PubMed DOI
Gray GR, Chauvin LP, Sarhan F, Huner NPA. Cold acclimation and freezing tolerance—a complex interaction of light and temperature. Plant Physiol. 1997;114:467–474. PubMed PMC
Griffith M, Yaish MWF. Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci. 2004;9:399–405. doi: 10.1016/j.tplants.2004.06.007. PubMed DOI
Griffith M, Lumb C, Ala P, Yang DSC, Hon W-C, Moffatt BA. Antifreeze protein produced endogenously in winter rye leaves. Plant Physiol. 1992;100:593–596. doi: 10.1104/pp.100.2.593. PubMed DOI PMC
Guo Y, Xiong L, Ishitani M, Zhu J-K. 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 USA. 2002;99:7786–7791. doi: 10.1073/pnas.112040099. PubMed DOI PMC
Gusta LV, O’Connor BJ, Gao YP, Jana S. A re-evaluation of controlled freeze-tests and controlled environment hardening conditions to estimate the winter survival potential of hardy winter wheats. Can J Plant Sci. 2001;81:241–246. doi: 10.4141/P00-068. DOI
Gusta LV, Wisniewski M, Nesbitt NT, Gusta ML. The effect of water, sugars, and proteins on the pattern of ice nucleation and propagation in acclimated and nonacclimated canola leaves. Plant Physiol. 2004;135:1642–1653. doi: 10.1104/pp.103.028308. PubMed DOI PMC
Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK. Metabolomics of temperature stress. Physiol Plantarum. 2008;132:220–235. PubMed
Hannah MA, Heyer AG, Hincha DK. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PloS Genet. 2005;1:179–196. doi: 10.1371/journal.pgen.0010026. PubMed DOI PMC
Hare PD, Cress WA, Van Staden J. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 1998;21:535–553. doi: 10.1046/j.1365-3040.1998.00309.x. DOI
Herman EM, Rotter K, Premakumar R, Elwinger G, Bae R, Ehler-King L, Chen S, Livingston DP., III Additional freeze hardiness in wheat acquired by exposure to −3°C is associated with extensive physiological, morphological, and molecular changes. J Exp Bot. 2006;57:3601–3618. doi: 10.1093/jxb/erl111. PubMed DOI
Hincha DK, Hagemann M. Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem J. 2004;383:277–283. doi: 10.1042/BJ20040746. PubMed DOI PMC
Iordachescu M, Imai R. Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol. 2008;50:1223–1229. doi: 10.1111/j.1744-7909.2008.00736.x. PubMed DOI
Irizarry RA, Hobbs B, Colin F, Beazer-Barclay YD, Antonellis K, Scherf U, Speed TP. Exploration, normalization and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249–264. doi: 10.1093/biostatistics/4.2.249. PubMed DOI
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. Quantification of plant frost injury by nonlinear fitting of an S-shaped function. Cryo-Lett. 1991;12:47–52.
Janas KM, Cvikrova M, Palagiewicz A, Eder J. Alterations in phenylpropanoid content in soybean roots during low temperature acclimation. Plant Physiol Biochem. 2000;38:587–593. doi: 10.1016/S0981-9428(00)00778-6. DOI
Kacperska A. Plant response to low temperature: signaling pathways involved in plant acclimation. In: Margesin R, Schinner F, editors. Cold-adapted organisms—ecology, physiology, enzymology and molecular biology. Berlin: Springer; 1999. pp. 79–103.
Kang J, Turano FJ. The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci USA. 2003;100:6872–6877. doi: 10.1073/pnas.1030961100. PubMed DOI PMC
Kaplan F, Guy CL. β-amylase induction and the protective role of maltose during temperature shock. Plant Physiol. 2004;135:1674–1684. doi: 10.1104/pp.104.040808. PubMed DOI PMC
Kaplan F, Sung DY, Guy CL. Roles of ß-amylase and starch breakdown during temperatures stress. Physiol Plantarum. 2006;126:120–128. doi: 10.1111/j.1399-3054.2006.00604.x. DOI
Kaul S, Sharma SS, Mehta IK. Free radical scavenging potential of L-proline: evidence from in vitro assays. Amino Acids. 2008;34:315–320. doi: 10.1007/s00726-006-0407-x. PubMed DOI
Koch K. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol. 2004;7:235–246. doi: 10.1016/j.pbi.2004.03.014. PubMed DOI
Kocsy G, Athmer B, Perovic D, Himmelbach A, Szűcs A, Vashegyi I, Schweizer P, Galiba G, Stein N. Regulation of gene expression by chromosome 5A during cold hardening in wheat. Mol Genet Genomics. 2010;283:351–363. doi: 10.1007/s00438-010-0520-0. PubMed DOI
Kovacs D, Kalmar E, Torok Z, Tompa P. Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol. 2008;147:381–390. doi: 10.1104/pp.108.118208. PubMed DOI PMC
Kumar SV, Wigge PA. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell. 2010;140:136–147. doi: 10.1016/j.cell.2009.11.006. PubMed DOI
Liu HL, Dai XY, Xu YY, Chong K. Over-expression of OsUGE-1 altered raffinose level and tolerance to abiotic stress but not morphology in Arabidopsis. J Plant Physiol. 2007;164:1384–1390. doi: 10.1016/j.jplph.2007.03.005. PubMed DOI
Livingston DP, III, Henson CA. Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol. 1998;116:403–408. doi: 10.1104/pp.116.1.403. DOI
Livingston D, Premakumar R, Tallury SP. Carbohydrate concentrations in crown fractions from winter oat during hardening at sub-zero temperatures. Ann Bot-London. 2005;96:331–335. doi: 10.1093/aob/mci167. PubMed DOI PMC
Livingston DP, Premakumar R, Tallury SP. Carbohydrate partitioning between upper and lower regions of the crown in oat and rye during cold acclimation and freezing. Cryobiology. 2006;52:200–208. doi: 10.1016/j.cryobiol.2005.11.001. PubMed DOI
Lunn JE, Feil R, Hendriks JH, Gibon Y, Morcuende R, Osuna D, Scheible WR, Carillo P, Hajirezaei MR, Stitt M. Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J. 2006;397:139–148. doi: 10.1042/BJ20060083. PubMed DOI PMC
Lunn J, Feil R, Yadav UP, Martins M, Ivakov A, Krause U, Wahl V, Stitt M (2010) Trehalose metabolism and sugar signalling in plants. XVII Congress of the Federation of European Societies of Plant Biology, Book of abstracts 4–9 July, Valencia, Spain
March-Díaz R, Reyes JC. The beauty of being a variant: H2A.Z and the SWR1 complex in plants. Mol Plant. 2009;2:565–577. doi: 10.1093/mp/ssp019. PubMed DOI
Mazzucotelli E, Tartari A, Cattivelli L, Forlani G. Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot. 2006;57:3755–3766. doi: 10.1093/jxb/erl141. PubMed DOI
Monroy A, Dryanova A, Malette B, Oren DH, Farajalla MR, Liu W, Danyluk J, Ubayasena LWC, Kane K, Scoles GJ, Sarhan F, Gulick PJ. Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Mol Biol. 2007;64:409–423. doi: 10.1007/s11103-007-9161-z. PubMed DOI
Ndong C, Danyluk J, Huner NPA, Sarhan F. Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure. Plant Mol Biol. 2001;45:691–703. doi: 10.1023/A:1010684719225. PubMed DOI
Nishizawa A, Yabuta Y, Shigeoka S. Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 2008;147:1251–1263. doi: 10.1104/pp.108.122465. PubMed DOI PMC
Novillo F, Alonso JM, Ecker JR, Salinas J. 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 USA. 2004;101:3985–3990. doi: 10.1073/pnas.0303029101. PubMed DOI PMC
Olenichenko NA, Zagoskina NV. Response of winter wheat to cold: production of phenolic compounds and L-phenylalanine ammonia lyase activity. Appl Biochem Microbiol. 2005;41:600–603. doi: 10.1007/s10438-005-0109-2. PubMed DOI
Olien CR. Freezing stress and survival. Annu Rev Plant Physiol. 1967;18:387–408. doi: 10.1146/annurev.pp.18.060167.002131. DOI
Paul M. Trehalose 6-phosphate. Curr Opin Plant Biol. 2007;10:303–309. doi: 10.1016/j.pbi.2007.04.001. PubMed DOI
Pearce RS, Houlston CE, Atherton KM, Rixon JE, Harrison P, Hughes MA, Dunn MA. Localization of expression of three cold-induced genes, blt101, blt4.9, and blt14, in different tissues of the crown and developing leaves of cold-acclimated cultivated barley. Plant Physiol. 1998;117:787–795. doi: 10.1104/pp.117.3.787. PubMed DOI PMC
Penfield S. Temperature perception and signal transduction in plants. New Phytol. 2008;179:615–628. doi: 10.1111/j.1469-8137.2008.02478.x. PubMed DOI
Pennycooke JC, Jones ML, Stushnoff C. Down-regulating alpha-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol. 2003;133:901–909. doi: 10.1104/pp.103.024554. PubMed DOI PMC
Pramanik MHR, Imai R. Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol. 2005;58:751–762. doi: 10.1007/s11103-005-7404-4. PubMed DOI
Prášil I, Zámečník J. 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. 1998;40:1–10. doi: 10.1016/S0098-8472(98)00010-0. DOI
Qin X, Zeevaart JAD. The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA. 1999;96:15354–15361. doi: 10.1073/pnas.96.26.15354. PubMed DOI PMC
Rapacz M, Plazek A, Niemczyk E. Frost de-acclimation of barley (Hordeum vulgare L.) and meadow fescue (Festuca pratensis Huds.). Relationship between soluble carbohydrate content and resistance to frost and the fungal pathogen Bipolaris sorokiniana (Sacc.) shoem. Ann Bot-London. 2000;86:539–545. doi: 10.1006/anbo.2000.1214. DOI
Renaut J, Hausman J-F, Wisniewski ME. Proteomics and low temperature studies: bridging the gap between gene expression and metabolism. Physiol Plantarum. 2006;126:97–109. doi: 10.1111/j.1399-3054.2006.00617.x. DOI
Rogers LA, Dubos C, Cullis IF, Surman C, Poole M, Willment J, Mansfield SD, Campbell MM. Light, the circadian clock, and sugar perception in the control of lignin biosynthesis. J Exp Bot. 2005;56:1651–1663. doi: 10.1093/jxb/eri162. PubMed DOI
Roitsch T, Gonzalez M-C. Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 2004;9:606–613. doi: 10.1016/j.tplants.2004.10.009. PubMed DOI
Rolland F, Baena-Gonzales E, Sheen J. Sugar sensing and signalling in plants: conserved and novel mechanisms. Annu Rev Plant Biol. 2006;57:675–709. doi: 10.1146/annurev.arplant.57.032905.105441. PubMed DOI
Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Guldener U, Mannhaupt G, Munsterkotter M, Mewes HW. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004;32:5539–5545. doi: 10.1093/nar/gkh894. PubMed DOI PMC
Salerno GL, Pontis HG. Raffinose synthesis in Chlorella vulgaris cultures after a cold shock. Plant Physiol. 1989;89:648–651. doi: 10.1104/pp.89.2.648. PubMed DOI PMC
Sangwan V, Örvar BL, Dhindsa RS. Early events during low temperature signaling. In: Li C, Palva ET, editors. Plant cold hardiness. Dordrecht: Kluwer Academic Publishers; 2002. pp. 43–53.
Sauer N. Molecular physiology of higher plant sucrose transporters. FEBS Lett. 2007;581:2309–2317. doi: 10.1016/j.febslet.2007.03.048. PubMed DOI
Skinner DZ. Post-acclimation transcriptome adjustment is a major factor in freezing tolerance of winter wheat. Funct Integr Genomics. 2009;9:513–523. doi: 10.1007/s10142-009-0126-y. PubMed DOI
Skinner JS, Von Zitzewitz J, Szűcs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM. Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol. 2005;59:533–551. doi: 10.1007/s11103-005-2498-2. PubMed DOI
Solecka D, Kacperska A. Phenylalanine ammonia-lyase activity in leaves of winter oilseed rape plants as affected by acclimation of plants to low temperature. Plant Physiol Biochem. 1995;33:585–591.
Sutton F, Chen DG, Ge X, Kenefick D. 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. 2009;9:34. doi: 10.1186/1471-2229-9-34. PubMed DOI PMC
Suzuki M, Kao CY, Cocciolone S, McCarty DR. Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J. 2001;28:409–418. doi: 10.1046/j.1365-313X.2001.01165.x. PubMed DOI
Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, Cattivelli L. Transcriptome analysis of cold acclimation in barley Albina and Xantha mutants. Plant Physiol. 2006;141:257–270. doi: 10.1104/pp.105.072645. PubMed DOI PMC
Tabaei-Aghdaei SR, Pearce RS, Harrison P. Sugars regulate cold-induced gene expression and freezing-tolerance in barley cell cultures. J Exp Bot. 2003;54:1565–1575. doi: 10.1093/jxb/erg173. PubMed DOI
Takahama U, Oniki T. A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells. Physiol Plantarum. 1997;101:845–852. doi: 10.1111/j.1399-3054.1997.tb01072.x. DOI
Talanova VV, Titov AF, Topchieva LV, Malysheva IE, Venzhik YV, Frolova SA. Expression of WRKY transcription factor and stress protein genes in wheat plants during cold hardening and ABA treatment. Russ J Plant Physiol. 2009;56:702–708. doi: 10.1134/S1021443709050173. DOI
Thimm O, Blaesing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004;37:914–939. doi: 10.1111/j.1365-313X.2004.02016.x. PubMed DOI
Timperio AM, Egidi MG, Zolla L. Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP) J Proteomics. 2008;71:391–411. doi: 10.1016/j.jprot.2008.07.005. PubMed DOI
Tommasini L, Svensson JT, Rodriguez EM, Wahid A, Malatrasi M, Kato K, Wanamaker S, Resnik J, Close TJ. Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.) Funct Integr Genomics. 2008;8:387–405. doi: 10.1007/s10142-008-0081-z. PubMed DOI
Trunova TI. Light and temperature systems in the hardening of winter wheat and the significance of oligosaccharides for frost resistance. Fiziol Rast. 1965;12:70–77.
Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y. Responses of the plasma membrane to low temperatures. Physiol Plantarum. 2006;126:81–89. doi: 10.1111/j.1399-3054.2005.00594.x. DOI
Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible W-R, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M. Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of coresponding genes, and comparison with known responses. Plant Physiol. 2005;138:1195–1204. doi: 10.1104/pp.105.060459. PubMed DOI PMC
Valluru R, Lammens W, Claupein W, Van den Ende W. Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Sci. 2008;13:409–414. doi: 10.1016/j.tplants.2008.05.008. PubMed DOI
Van Buskirk HA, Thomashow MF. Arabidopsis transcription factors regulating cold acclimation. Physiol Plantarum. 2006;126:72–80. doi: 10.1111/j.1399-3054.2006.00625.x. DOI
Vaultier M-N, Cantrel C, Vergnolle C, Justin A-M, Demandre C, Benhassaine-Kesri G, Cicek D, Zachowski A, Ruelland E. Desaturase mutants reveal that membrane rigidification acts as a cold perception mechanism upstream of the diacylglycerol kinase pathway in Arabidopsis cells. FEBS Lett. 2006;580:4218–4223. doi: 10.1016/j.febslet.2006.06.083. PubMed DOI
Vogel G, Aeschbacher RA, Müller J, Boller T, Wiemken A. Trehalose-6-phosphate phosphatases from Arabidopsis thaliana: identification by functional complementation of yeast tps2 mutant. Plant J. 1998;13:673–683. doi: 10.1046/j.1365-313X.1998.00064.x. PubMed DOI
Wang X, Li W, Li M, Welti R. Profiling lipid changes in plant response to low temperatures. Physiol Plantarum. 2006;126:90–96. doi: 10.1111/j.1399-3054.2006.00622.x. DOI
Whetten R, Sederoff R. Lignin biosynthesis. Plant Cell. 1995;7:1001–1013. doi: 10.1105/tpc.7.7.1001. PubMed DOI PMC
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ. Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J. 2010;8:749–771. doi: 10.1111/j.1467-7652.2010.00536.x. PubMed DOI
Wisniewski M, Fuller M. Ice nucleation and deep supercooling in plants: new insights using infrared thermography. In: Margesin R, Schinner F, editors. Cold-adapted organisms—ecology, physiology, enzymology and molecular biology. Berlin: Springer; 1999. pp. 105–118.
Wisniewski M, Webb R, Balsamo R, Close TJ, Yu X-M, Griffith M. Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica) Physiol Plantarum. 1999;105:600–608. doi: 10.1034/j.1399-3054.1999.105402.x. DOI
Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stress. Annu Rev Plant Biol. 2006;57:781–803. doi: 10.1146/annurev.arplant.57.032905.105444. PubMed DOI
Yano R, Nakamura M, Yoneyama T, Nishida I. Starch related α-glucan/water dikinase is involved in the cold induced development of freezing tolerance in Arabidopsis. Plant Physiol. 2005;138:837–846. doi: 10.1104/pp.104.056374. PubMed DOI PMC
Zámečník J, Bieblová J, Grospietsch M. Safety zone as a barrier to root-shoot ice propagation. Plant Soil. 1994;167:149–155. doi: 10.1007/BF01587610. DOI
Zuther E, Buchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG. The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett. 2004;576:169–173. doi: 10.1016/j.febslet.2004.09.006. PubMed DOI
Plant Proteoforms Under Environmental Stress: Functional Proteins Arising From a Single Gene
Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways
Plant Abiotic Stress Proteomics: The Major Factors Determining Alterations in Cellular Proteome