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Published September 30, 2015 | Version v1
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Low temperature tolerance in plants: Changes at the protein level

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  • 1. Department of Agronomy and Plant Breeding, Agriculture College, University of Maragheh, Iran

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Janmohammadi, Mohsen, Zolla, Lello, Rinalducci, Sara (2015): Low temperature tolerance in plants: Changes at the protein level. Phytochemistry 117: 76-89, DOI: 10.1016/j.phytochem.2015.06.003, URL: http://dx.doi.org/10.1016/j.phytochem.2015.06.003

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urn:lsid:plazi.org:pub:63192A35FD12FFCC0203FFCEFFAFB22B

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Publication: 10.1111/ppl.12291 (DOI)
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Figure: 10.5281/zenodo.10486649 (DOI)
Figure: 10.5281/zenodo.10486651 (DOI)

References

  • Baxter, H.L., Stewart Jr, C.N., 2013. Effects of altered lignin biosynthesis on phenylpropanoid metabolism and plant stress. Biofuels 4, 635-650.
  • Breton, G., Danyluk, J., Charron, J.B.F., Sarhan, F., 2003. Expression profiling and bioinformatic analyses of a novel stress-regulated multispanning transmembrane protein family from cereals and arabidopsis. Plant Physiol. 132, 64-74.
  • Campbell, S.A., Close, T.J., 1997. Dehydrins: genes, proteins, and association with phenotypic traits. New Phytol. 137, 61-74.
  • Checker, V.G., Chhibbar, A.K., Khurana, P., 2012. Stress-inducible expression of barley Hva1 gene in transgenic mulberry displays enhanced tolerance against drought, salinity and cold stress. Transgenic Res. 21, 939-957.
  • Chen, J., Tian, L., Xu, H., Tian, D., Luo, Y., Ren, C., Yang, L., Shi, J., 2012. Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis. Plant Omics 5, 194-199.
  • Cheng, N.H., Pittman, J.K., Barkla, B.J., Shigaki, T., Hirschi, K.D., 2003. The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell. 15, 347-364.
  • Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B., Hong, X., Agarwal, M., Zhu, J.K., 2003. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genet Dev. 17, 1043-1054.
  • Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444-452.
  • Chinnusamy, V., Zhu, J.K., Sunkar, R, 2010. Gene regulation during cold stress acclimation in plants. Methods Mol. Biol. 639, 39-55.
  • Cho, M.R., Lee, K.H., Hyun, Y., Lee, I., Kim, H.J., 2007. Proteome analysis of vernalization-treated Arabidopsis thaliana by matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry. Bull. Korean Chem. Soc. 28, 427- 431.
  • Christov, N.K., Imai, R., Blume, Y., 2008. Differential expression of two winter wheat alpha-tubulin genes during cold acclimation. Cell Biol. Int. 32, 574-578.
  • Ciannamea, S., Kaufmann, K., Frau, M., Tonaco, I.A., Petersen, K., Nielsen, K.K., Angenent, G.C., Immink, R.G., 2006. Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne. J. Exp. Bot. 57, 3419-3431.
  • Conde, A., Chaves, M.M., Geros, H., 2011. Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52, 1583-1602.
  • Crosatti, C., Pagani, D., Cattivelli, L., Stanca, A.M., Rizza, F., 2008. Effects of growth stage and hardening conditions on the association between frost resistance and the expression of the cold-induced protein COR14b in barley. Environ. Exp. Bot. 62, 93-100.
  • Crosatti, C., Rizza, F., Badeck, F.W., Mazzucotelli, E., Cattivelli, L., 2013. Harden the chloroplast to protect the plant. Physiol. Plantarum 147, 55-63.
  • Cui, S., Huang, F., Wang, J., Ma, X., Cheng, Y., Liu, J., 2005. A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5, 3162-3172.
  • Dal Bosco, C., Busconi, M., Govoni, C., Baldi, A.M., Crosatti, C., Bassi, R., Cattivelli, L., 2003. Cor gene expression in barley mutants affected in chloroplast development and photosynthetic electron transport. Plant Physiol. 131, 793- 802.
  • Dong, C.H., Agarwal, M., Zhang, Y., Xie, Q., Zhu, J.K., 2006. The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. PNAS 103, 8281-8286.
  • Fan, J., Ren, J., Zhu, W., Amombo, E., Fu, J., Chen, L., 2014. Antioxidant responses and gene expression in bermudagrass under cold stress. J. Am. Soc. Hortic. Sci. 139, 699-705.
  • Fanucchi, F., Alpi, E., Olivieri, S., Cannistraci, C.V., Bachi, A., Alpi, A., Alessio, M., 2012. Acclimation increases freezing stress response of Arabidopsis thaliana at proteome level. Biochim. Biophys. Acta. 1824, 813-825.
  • FAO, 2008 FAOSTAT, Food and Agriculture Organization of the United Nations Rome, Italy. Available at: http://faostat.fao.org.
  • Gharechahi, J., Alizadeh, H., Naghavi, M.R., Sharifi, G., 2014. A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.). Mol. Biol. Rep. 41, 3897-3905.
  • Gillet, L.C., Navarro, P., Tate, S., Rost, H., Selevsek, N., Reiter, L., Bonner, R., Aebersold, R., 2012. Targeted data extraction of the MS/MS spectra generated by dataindependent acquisition: a new concept for consistent and accurate proteome analysis. Mol. Cell. Proteomics 11 (O111), 016717.
  • 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. Bioch. 63, 236-244.
  • Hashimoto, M., Komatsu, S., 2007. Proteomic analysis of rice seedlings during cold stress. Proteomics 7, 1293-1302.
  • Hashimoto, M., Toorchi, M., Matsushita, K., Iwasaki, Y., Komatsu, S., 2009. Proteome analysis of rice root plasma membrane and detection of cold stress responsive proteins. Protein Pept. Lett. 16, 685-697.
  • Herman, E.M., Rotter, K., Premakumar, R., Elwinger, G., Bae, R., Ehler-King, L., Chen, S., Livingston, D.P., 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.
  • Hlavackova, I., Vitamvas, P., Santrucek, J., Kosova, K., Zelenkova, S., Prasil, I.T., Ovesna, J., Hynek, R., Kodicek, M., 2013. Proteins involved in distinct phases of cold hardening process in frost resistant winter barley (Hordeum vulgare l.) cv luxor. Int. J. Mol. Sci. 14, 8000-8024.
  • Hu, W., Hu, G., Han, B., 2009. Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci. 176, 583-590.
  • Imin, N., Kerim, T., Rolfe, B.G., Weinman, J.J., 2004. Effect of early cold stress on the maturation of rice anthers. Proteomics 4, 1873-1882.
  • Jahanbakhsh-Godehkahriz, S., Rastgar-Jazii, F., Zolla, L., Karimzadeh, G., Mahfoozi, S., Hosseini-Salekdeh, G., Gholipoori, A., Jahanbakhsh-Godehkahriz, S., 2011. Analysis and identification of cold responsive proteins in Kohdasht spring wheat (Triticum aestivum). Proc. Comput. Sci. 3, 70-73.
  • Janmohammadi, M., Enayati, V., Sabaghnia, N., 2012. Impact of cold acclimation, deacclimation and re-acclimation on carbohydrate content and antioxidant enzyme activities in spring and winter wheat. Icel. Agric. Sci. 25, 3-11.
  • Janmohammadi, M., Matros, A., Mock, H.P., 2014. Proteomic analysis of cold acclimation in winter wheat under field condition. Icel. Agric. Sci. 27, 3-15.
  • Janska, A., Aprile, A., Zamecnik, J., Cattivelli, L., Ovesna, 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.
  • Jeon, J., Kim, J., 2013. Cold stress signaling networks in Arabidopsis. Plant Biol. 56, 69-76.
  • Jing, C., Jing, Y., Li-jie, L., Yang, Y., Hong, C., Zai-bin, H., Zhuo-fu, L., 2012. Two-dimensional electrophoresis analysis of proteins in response to cold stress in extremely cold-resistant winter wheat Dongnongdongmai 1 tillering nodes. J. Northeast Agri. Uni. 19, 27-35.
  • Karlson, D., Nakaminami, K., Toyomasu, T., Imai, R., 2002. A cold-regulated nucleic acid-binding protein of winter wheat shares a domain with bacterial cold shock proteins. J. Biol. Chem. 277, 35248-35256.
  • Kawamura, Y., Uemura, M., 2003. Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36, 141-154.
  • Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., Harter, K., 2007. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50, 347-363.
  • Kocsy, G., Athmer, B., Perovic, D., Himmelbach, A., 2010. Regulation of gene expression by chromosome 5A during cold hardening in wheat. Mol. Genet. Genomics 283, 351-363.
  • Komatsu, S., Yamada, E., Furukawa, K., 2009. Cold stress changes the concanavalin A-positive glycosylation pattern of proteins expressed in the basal parts of rice leaf sheaths. Amino Acids 36, 115-123.
  • Kosova, K., Prasil, I.T., Vitamvas, P., Dobrev, P., Motyka, V., Flokova, K., Vankova, R., 2012. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J. Plant Physiol. 169, 567-576.
  • Kosova, K., Vitamvas, P., Prasil, I.T., Renaut, J., 2011. Plant proteome changes under abiotic stress - contribution of proteomics studies to understanding plant stress response. J. Proteomics 74, 1301-1322.
  • Kosova, K., Vitamvas, P., Planchon, S., Renaut, J., Vankova, R., Prasil, I.T., 2013a. 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.
  • Kosova, K., Vitamvas, P., Prasilova, P., Prasil, I.T., 2013b. Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale. Biol. Plantarum 57, 105-112.
  • Kosova, K., Vitamvas, P., Prasil, I.T., 2014a. Proteomics of stress responses in wheat and barley-search for potential protein markers of stress tolerance. Front. Plant Sci. 5, 711.
  • Kosova, K., Vitamvas, P., Prasil, I.T., 2014b. Wheat and barley dehydrins under cold, drought, and salinity-what can LEA-II proteins tell us about plant stress response? Front. Plant Sci. 5, 343.
  • Lang, V., Palva, E.T., 1992. The expression of a rab-related gene, rab18, is induced by abscisic acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 20, 951-962.
  • Larcher, W., 2003. Plants under stress. In: Physiological Plant Ecology. Ecophysiology and Stress of Functional Groups, fourth ed. Springer, Berlin, Heidelberg, pp. 345-450.
  • Larkindale, J., Knight, M.R., 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128, 682-695.
  • Le, M.Q., Engelsberger, W.R., Hincha, D.K., 2008. Natural genetic variation in acclimation capacity at sub-zero temperatures after cold acclimation at 4 °C in different Arabidopsis thaliana accessions. Cryobiology 57, 104-112.
  • Lee, D.G., Ahsan, N., Lee, S.H., Kang, K.Y., Lee, J.J., Lee, B.H., 2007. An approach to identify cold-induced low-abundant proteins in rice leaf. C. R. Biol. 330, 215- 225.
  • Lee, H., Xiong, L., Gong, Z., Ishitani, M., Stevenson, B., Zhu, J.K., 2001. The Arabidopsis HOS1gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev. 15, 912-924.
  • Lee, B.H., Lee, H., Xiong, L., Zhu, J.K., 2002. A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14, 1235-1251.
  • Less, H., Galili, G., 2008. Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant physiol. 147, 316-330.
  • Lehmann, U., Wienkoop, S., Tschoep, H., Weckwerth, W., 2008. If the antibody fails-a mass western approach. Plant J. 55, 1039-1046.
  • Li, X., Cai, J., Liu, F., Dai, T., Cao, W., Jiang, D., 2014. Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature. Funct. Plant Biol. 41, 690-703.
  • Limin, A., Fowler, D.B., 2006. Low-temperature tolerance and genetic potential in wheat (Triticum aestivum L.): response to photoperiod, vernalization, and plant development. Planta 224, 360-366.
  • Liu, H., Ouyang, B., Zhang, J., Wang, T., Li, H., Zhang, Y., Yu, C., Ye, Z., 2012. Differential modulation of photosynthesis, signaling, and transcriptional regulation between tolerant and sensitive tomato genotypes under cold stress. PLoS One 7, e50785.
  • Lopez-Matas, M.A., Nunez, P., Soto, A., Allona, I., Casado, R., Collada, C., Guevara, M.A., Aragoncillo, C., Gomez, L., 2004. Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiol. 134, 1708-1717.
  • Miura, K., Furumoto, T., 2013. Cold signaling and cold response in plants. Int. J. Mol. Sci. 14, 5312-5337.
  • Mutlu, S., Karadagoglu, O., Atici, O., Nalbantoglu, B., 2013. Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol. Plantarum 57, 507-513.
  • Neilson, K.A., Mariani, M., Haynes, P.A., 2011. Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics 11, 1696-1706.
  • Ohnishi, T., Nakazono, M., Tsutsumi, N., 2008. Abiotic stress. In: Biotechnology in Agriculture and Forestry. In: Hirano, H.Y., Hirai, A., Sano, Y., Sasaki, T. (Eds.), . Rice Biology in the Genomics Era IV, vol. 62. Springer, Heidelberg, pp. 337-355.
  • Ouellet, F., Carpentier, E., Cope, M., Monroy, A.F., Sarhan, F., 2001. Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiol. 125, 360-368.
  • Pino, M.T., Skinner, J.S., Jeknic, Z., Park, E.J., Hayes, P.M., Chen, T.H.H., 2006. Ectopic overexpression of AtCBF1 in potato enhances freezing tolerance. In: Chen, T.H.H., Uemura, M., Fujikawa, S. (Eds.), Cold Hardiness in Plants: Molecular Genetics, Cell Biology, and Physiology. CABI Publishing, Oxfordshire, UK, pp. 103-123.
  • Reyes-Diaz, M., Ulloa, N., Zuniga-Feest, A., Gutierrez, A., Gidekel, M., Alberdi, M., Corcuera, L.J., Bravo, L.A., 2006. Arabidopsis thaliana avoids freezing by supercooling. J. Exp. Bot. 57, 3687-3696.
  • Rinalducci, S., Egidi, M.G., Karimzadeh, G., Rastgar-Jazii, F., Zolla, L., 2011a. Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis 32, 1807-1818.
  • Rinalducci, S., Egidi, M.G., Mahfoozi, S., Jahanbakhsh, S., Zolla, L., 2011b. The influence of temperature on plant development in a vernalization-requiring winter wheat: a 2-DE based proteomic investigation. J. Proteomics 74, 643-659.
  • Rocco, M., Arena, S., Renzone, G., Scippa, G.S., Lomaglio, T., Verrillo, F., Scaloni, A., Marra, M., 2013. Proteomic analysis of temperature stress-responsive proteins in Arabidopsis thaliana rosette leaves. Mol. Biosyst. 9, 1257-1267.
  • Saibo, N.J.M., Lourenc, T., Oliveira, M.M., 2009. Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann. Bot. 103, 609-623.
  • Sangwan, V., Foulds, I., Singh, J., Dhindsa, R.S., 2001. Cold-activation of Brassica napus BN 115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J. 27, 1-12.
  • Sarhadi, E., Mahfoozi, S., Hosseini, S.A., Salekdeh, G.H., 2010. Cold acclimation proteome analysis reveals close link between up-regulation of low-temperature associated proteins and vernalization fulfillment. J. Proteome Res. 9, 5658-5667.
  • Singh, R., Jwa, N., 2013. Understanding the responses of rice to environmental stress using proteomics. J. Proteomic Res. 12, 4652-4669.
  • Soltesz, A., Smedley, M., Vashegyi, I., Galiba, G., Harwood, W., Vagujfalvi, A., 2013. Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance. J. Exp. Bot. 64, 1849-1862.
  • Suzuki, N., Mittler, R., 2006. Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiol. Plantarum. 126, 45-51.
  • Svensson, J., Ismail, A.M., Palva, E.T., Close, T.J., 2002. Dehydrins. In: Storey, K.B., Storey, J.M. (Eds.), Sensing, Signaling and Cell Adaptation. Elsevier Science B. V., pp. 155-171.
  • Svensson, J.T., Crosatti, C., Campoli, C., Bassi, R., Stanca, A.M., Close, T.J., Cattivelli, L., 2006. Transcriptome analysis of cold acclimation in barley Albina and Xantha mutants. Plant Physiol. 141, 257-270.
  • Sze, H., Liang, F., Hwang, I., Curran, A.C., Harper, J.F., 2000. Diversity and regulation of plant Ca2+ pumps: insights from expression in yeast. Annu. Rev. Plant Biol. 51, 433-462.
  • Tenhaken, R., 2015. Cell wall remodeling under abiotic stress. Front. Plant Sci. 5, 771.
  • Thomashow, M.F., 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Phys. 50, 571-599.
  • Timperio, A.M., Egidi, M.G., Zolla, L., 2008. Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J. Proteomics 71, 391-411.
  • Toptikov, V.A., D'yachenko, L.F., Totskii, V.N., 2012. Expression of antioxidant oxidoreductases and protein profile of seedling tissues of winter and spring forms of cereals under extreme temperature fluctuations. Cytol. Genet. 46, 161-171.
  • Trevaskis, B., 2010. The central role of the VERNALIZATION1 gene in the vernalization response of cereals. Funct. Plant Biol. 37, 479-487.
  • Uemura, M., Tominaga, Y., Nakagawara, C., Shigematsu, S., Minami, A., Kawamura, Y., 2006. Responses of the plasma membrane to low temperatures. Physiol. Plantarum. 126, 81-89.
  • Vitamvas, P., Prasil, I.T., Kosova, K., Planchon, S., Renaut, J., 2012. Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics 12, 68-85.
  • von Zitzewitz, J., Sz ucs } , P., Dubcovsky, J., Yan, L., Francia, E., Pecchioni, N., Casas, A., Chen, T.H.H., Hayes, P.M., Skinner, J.S., 2005. Molecular and structural characterization of barley vernalization genes. Plant Mol. Biol. 59, 449-467.
  • Wang, W., Vinocur, B., Shoseyov, O., Altman, A., 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9, 244-252.
  • Weckwerth, W., Baginsky, S., vanWijk, K., Heazlewood, J.L., Millar, H., 2008. The multinational arabidopsis steering subcommittee for proteomics assembles the largest proteome database resource for plant systems biology. J. Proteome Res. 7, 4209-4210.
  • Winfield, M.O., Lu, C., Wilson, I.D., Coghill, J.A., Edwards, K.J., 2010. Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol. J. 8, 749-771.
  • Xu, J., Li, Y., Sun, J., Du, L., Zhang, Y., Yu, Q., Liu, X., 2013. Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biol. 15, 292-303.
  • 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.
  • Yun, K.Y., Park, M.R., Mohanty, B., Herath, V., Xu, F., Mauleon, R., Wijaya, E., Bajic, V.B., Bruskiewich, R., de los Reyes, B.G., 2010. Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol. 10, 16.
  • Zabotin, A.I., Barisheva, T.S., Trofimova, O.I., Toroschina, T.E., Larskaya, I.A., Zabotina, O.A., 2009. Oligosaccharin and ABA synergistically affect the acquisition of freezing tolerance in winter wheat. Plant Physiol Biochem. 47, 854-858.
  • Zeng, Y., Yu, J., Cang, J., Liu, L., Mu, Y., Wang, J., Zhang, D., 2011. Detection of sugar accumulation and expression levels of correlative key enzymes in winter wheat (Triticum aestivum) at low temperatures.Biosci.Biotechnol.Biochem. 75,681-687.
  • Zhang, S., Song, G., Li, Y., Jie, G., Wang, J., Chen, G., Li, H., Li, G., Zhao, Z., 2014. Comparative proteomic analysis of cold responsive proteins in two wheat cultivars with different tolerance to spring radiation frost. Front. Agr. Sci. Eng. 1, 37-45.
  • Zhang, T., Zhao, X., Wang, W., Pan, Y., Huang, L., Liu, X., Zong, Y., Zhu, L., Yang, D., Fu, B., 2012. Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. PLoS One 7, e43274.
  • Zhao, J., Zhang, S., Yang, T., Zeng, Z., Huang, Z., Liu, Q., Wang, X., Leach, J., Leung, H., Liu, B., 2014. Global transcriptional profiling of a cold-tolerant rice variety under moderate cold stress reveals different cold stress response mechanisms. Physiol. Plantarum. http://dx.doi.org/10.1111/ppl.12291.