Abstract
To gain a better understanding of cold acclimation process in wheat, we applied a 2-DE based proteomic approach to discover changes in proteome profile of a diploid wild wheat (Triticum urartu L.) during prolonged cold stress treatment. To this end, plants were grown in pots and the growing seedlings (4-leaf stage) were exposed to cold stress. After 4 weeks of cold acclimation (4–6 °C) and subsequent treatment for 12 h at −2 °C, samples were collected from control and stressed plants and were subjected to proteome pattern analysis. Among approximately 450 reproducible protein spots displayed in each given 2-DE gels, 34 proteins changed significantly in abundance in response to cold stress. Among them, 25 and 9 proteins were up and down-regulated under stress condition, respectively. Analysis by matrix-assisted laser desorption ionization time of flight/time of flight mass spectrometry coupled with non-redundant protein database search allowed the identification of 20 cold-induced proteins. Integrated proteomic and database survey resulted in identification of several cold stress related proteins such as pathogenesis related protein, cold regulated protein, cold-responsive LEA/RAB-related COR protein, oxygen-evolving enhancer protein and oxalate oxidase. The presumed functions of the identified proteins were mostly related to cold acclimation, oxidative stress and photosynthesis. The possible implications of differentially accumulated proteins in acquiring systemic tolerance to freezing stress following exposure to prolonged low temperature will be discussed.
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References
Hale MG, Orcutt DM (1987) The physiology of plants under stress. Wiley, New York
Yadav S (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Dev 30:515–527
Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223
Atici O, Nalbantoglu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196
Griffith M, Antikainen M, Hon W-C, Pihakaski-Maunsbach K, Yu X-M, Chun JU, Yang DSC (1997) Antifreeze proteins in winter rye. Physiol Plant 100:327–332
Janská A, Maršík P, Zelenková S, Ovesná J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405
Xin Z (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902
Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 109:15–30
Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low-temperature response in plants. BioEssays 27:1048–1059
Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
Renaut J, Hausman JF, Wisniewski ME (2006) Proteomics and low‐temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109
Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt osmotic, and cold stress. Plant Physiol 130:2129–2141
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 Online 14:1675–1690
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high‐salinity stresses using a full‐length cDNA microarray. Plant J 31:279–292
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Fujita M, Yoshiwara K, Matsukura S, Morishita Y, Sasaki R, Suzuki H, Saito K, Shibata D, Shinozaki K, Yamaguchi-Shinozaki K (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150:1972–1980
Greenbaum D, Colangelo C, Williams K, Gerstein M (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117
Pradet-Balade B, Boulme F, Beug H, Mullner EW, Garcia-Sanz JA (2001) Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 26:225–229
Rinalducci S, Egidi MG, Mahfoozi S, Godehkahriz SJ, Zolla L (2011) The influence of temperature on plant development in a vernalization-requiring winter wheat: a 2-DE based proteomic investigation. J Proteomics 74:643–659
Kosová K, Vítámvás P, Planchon S, Renaut J, Vanková R, Prášil IT (2013) Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. J Proteome Res 12:4830–4845
Wang X, Yang P, Zhang X, Xu Y, Kuang T, Shen S, He Y (2009) Proteomic analysis of the cold stress response in the moss Physcomitrella patens. Proteomics 9:4529–4538
Sarhadi E, Mahfoozi S, Hosseini SA, Salekdeh GH (2010) Cold acclimation proteome analysis reveals close link between the up-regulation of low-temperature associated proteins and vernalization fulfillment. J Proteome Res 9:5658–5667
Brule-Babel AL, Fowler DB (1988) Genetic control of cold hardiness and vernalization requirement in winter wheat. Crop Sci 28:879–884
Damerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Gharechahi J, Khalili M, Hasanloo T, Salekdeh GH (2013) An integrated proteomic approach to decipher the effect of methyl jasmonate elicitation on the proteome of Silybum marianum L. hairy roots. Plant Physiol Biochem 70:115–122
Blum H, Beier H, Gross HJ (1987) Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis (Weinheim, Fed. Repub. Ger.) 8:93–99
Sharifi G, Ebrahimzadeh H, Ghareyazie B, Gharechahi J, Vatankhah E (2012) Identification of differentially accumulated proteins associated with embryogenic and non-embryogenic calli in saffron (Crocus sativus L.). Proteome Sci 10:3
Fowler DB, Limin AE, Ritchie JT (1999) Low-temperature tolerance in cereals: model and genetic interpretation. Crop Sci 39:626–633
Olien CR (1967) Freezing stresses and survival. Annu Rev Plant Physiol 18:387–408
Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508
Renaut J, Hausman J-F, Wisniewski ME (2006) Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109
Pomeroy MK, Fowler DB (1973) Use of lethal dose temperature estimates as indices of frost tolerance for wheat cold acclimated under natural and controlled environments. Can J Plant Sci 53:489–494
Kobayashi F, Takumi S, Nakata M, Ohno R, Nakamura T, Nakamura C (2004) Comparative study of the expression profiles of the Cor/Lea gene family in two wheat cultivars with contrasting levels of freezing tolerance. Physiol Plant 120:585–594
Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638
Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118
NDong C, Danyluk J, Wilson KE, Pocock T, Huner NP, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368–1381
Tsuda K, Tsvetanov S, Takumi S, Mori N, Atanassov A, Nakamura C (2000) New members of a cold-responsive group-3 Lea/Rab-related Cor gene family from common wheat (Triticum aestivum L.). Genes Genet Syst 75:179–188
Xu D, Duan X, Wang B, Hong B, Ho T, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1 from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257
Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant group 2 and group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611–616
Yu J-N, Zhang J-S, Shan L, Chen S-Y (2005) Two new group 3 LEA genes of wheat and their functional analysis in yeast. J Integr Plant Biol 47:1372–1381
Rinalducci S, Egidi MG, Karimzadeh G, Jazii FR, Zolla L (2011) Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis 32:1807–1818
Han Q, Kang G, Guo T (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244
Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:26
Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. CMLS Cell Mol Life Sci 57:779–795
McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848
Gupta AS, Webb RP, Holaday AS, Allen RD (1993) Overexpression of superoxide dismutase protects plants from oxidative stress (induction of ascorbate peroxidase in superoxide dismutase-overexpressing plants). Plant Physiol 103:1067–1073
Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181
May MJ, Vernoux T, Leaver C, Montagu MV, Inzé D (1998) Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49:649–667
Yan S-P, Zhang Q-Y, Tang Z-C, Su W-A, Sun W-N (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484–496
Bocian A, Kosmala A, Rapacz M, Jurczyk B, Marczak L, Zwierzykowski Z (2011) Differences in leaf proteome response to cold acclimation between Lolium perenne plants with distinct levels of frost tolerance. J Plant Physiol 168:1271–1279
Hahn M, Walbot V (1989) Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiol 91:930–938
Dorrestein PC, Huili ZH, Taylor SV, McLafferty FW, Begley TP (2004) The biosynthesis of the thiazole phosphate moiety of thiamin (vitamin B1): the early steps catalyzed by thiazole synthase. J Am Chem Soc 126:3091–3096
Hohmann S, Meacock PA (1998) Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochimica et Biophysica Acta (BBA) 1385:201–219
Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D (2009) Thiamin confers enhanced tolerance to oxidative stress in arabidopsis. Plant Physiol 151:421–432
Sayed SA, Gadallah MAA (2002) Effects of shoot and root application of thiamin on salt-stressed sunflower plants. Plant Growth Regul 36:71–80
Ribeiro DT, Farias LP, de Almeida JD, Kashiwabara PM, Ribeiro AFC, Silva-Filho MC, Menck CFM, Van Sluys M-A (2005) Functional characterization of the THI1 promoter region from Arabidopsis thaliana. J Exp Bot 56:1797–1804
Vítámvás P, Saalbach G, Prášil IT, Čapková V, Opatrná J, Ahmed J (2007) WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J Plant Physiol 164:1197–1207
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This work was supported by a grant provided by department of agronomy and plant breeding at University College of Agriculture and Natural resources, University of Tehran.
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Gharechahi, J., Alizadeh, H., Naghavi, M.R. et al. A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.). Mol Biol Rep 41, 3897–3905 (2014). https://doi.org/10.1007/s11033-014-3257-8
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DOI: https://doi.org/10.1007/s11033-014-3257-8