Cold stress, as chilling (<20 °C) or freezing (<0 °C), is one of the frequently exposed stresses in cultivated plants like potato. Under cold stress, plants differentially modulate their gene expression to develop a cold tolerance/acclimation. In the present study, we aimed to identify the overall gene expression profile of chilling-stressed (+4 °C) potato at four time points (4, 8, 12, and 48 h), with a particular emphasis on the genes related with transcription factors (TFs), phytohormones, lipid metabolism, signaling pathway, and photosynthesis. A total of 3504 differentially expressed genes (DEGs) were identified at four time points of chilling-induced potato, of which 1397 were found to be up-regulated while 2107 were down-regulated. Heatmap showed that genes were mainly up-regulated at 4-, 8-, and 12-h time points; however, at 48-h time point, they inclined to down-regulate. Seventy five up-regulated TF genes were identified from 37 different families/groups, including mainly from bHLH, WRKY, CCAAT-binding, HAP3, and bZIP families. Protein kinases and calcium were major signaling molecules in cold-induced signaling pathway. A collaborated regulation of phytohormones was observed in chilling-stressed potato. Lipid metabolisms were regulated in a way, highly probably, to change membrane composition to avoid cold damage and render in signaling. A down-regulated gene expression profile was observed in photosynthesis pathway, probably resulting from chilling-induced reduced enzyme activity or light-triggered ROSs damage. The findings of this study will be a valuable theoretical knowledge in terms of understanding the chilling-induced tolerance mechanisms in cultivated potato plants as well as in other Solanum species.
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Evers, D., Bonnechère, S., Hoffmann, L., & Hausman, J. F. (2007). Physiological aspects of abiotic stress response in potato. Belgian Journal of Botany, 141–150.
Jefferies, R. A., & MacKerron, D. K. L. (1993). Responses of potato genotypes to drought. II. Leaf area index, growth and yield. Annals of Applied Biology, 122(1), 105–112.
Chinnusamy, V., Zhu, J. K., & Sunkar, R. (2010). Gene regulation during cold stress acclimation in plants. In R. Sunkar (Ed.), Plant stress tolerance. Methods in Molecular Biology, 639 (pp. 39–55). Totowa, NJ: Humana Press.
Floris, M., Hany, M., Elodie, L., Christophe, R., & Benoit, M. (2009). Post-transcriptional regulation of gene expression in plants during abiotic stress. International Journal of Molecular Sciences, 10, 3168–3185.
Le, M. Q., Pagter, M., & Hincha, D. K. (2015). 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 Molecular Biology, 87(1-2), 1–15.
Oufir, M., Legay, S., Nicot, N., Van, M. K., Hoffmann, L., Renaut, J., Hausman, J. F., & Evers, D. (2008). Gene expression in potato during cold exposure: changes in carbohydrate and polyamine metabolisms. Plant Science, 175, 839–852.
Chawade, A., Lindlöf, A., Olsson, B., & Olsson, O. (2013). Global expression profiling of low temperature induced genes in the chilling tolerant japonica rice Jumli Marshi. PLoS One, 8(12), e81729.
Laudencia-Chingcuanco, D., Ganeshan, S., You, F., Fowler, B., Chibbar, R., & Anderson, O. (2011). Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L.). BMC Genomics, 12, 299.
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 Physiology, 141, 257–270.
Chawade, A., Linden, P., Brautigam, M., Jonsson, R., Jonsson, A., Moritz, T., & Olsson, O. (2012). Development of a model system to identify differences in spring and winter oat. PLoS One, 7, e29792.
Fowler, S., & Thomashow, M. F. (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.
Evers, D., Legay, S., Lamoureux, D., Hausman, J. F., Hoffmann, L., & Renaut, J. (2012). Towards a synthetic view of potato cold and salt stress response by transcriptomic and proteomic analyses. Plant Molecular Biology, 78(4-5), 503–514.
Solanke, A. U., & Sharma, A. K. (2008). Signal transduction during cold stress in plants. Physiology and Molecular Biology of Plants, 14(1-2), 69–79.
Chinnusamy, V., Zhu, J., & Zhu, J. K. (2007). Cold stress regulation of gene expression in plants. Trends in Plant Science, 12, 444–451.
Renaut, J., Planchon, S., Oufir, M., Hausman, J. F., Hoffmann, L., & Evers, D. (2009). , Identification of proteins from potato leaves submitted to chilling temperature. In L. V. Gusta, M. Wisniewski, & K. K. Tanino (Eds.), Plant cold hardiness: from the laboratory to the field (pp. 279–292). Wallingford: CAB Internationnal.
Guy, C., Kaplan, F., Kopka, J., Selbig, J., & Hincha, D. K. (2008). Metabolomics of temperature stress. Physiologia Plantarum, 132, 220–235.
Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant Journal, 45, 523–539.
Shinozaki, K., Yamaguchi-Shinozaki, K., & Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology, 6, 410–417.
Nakashima, K., & Yamaguchi-Shinozaki, K. (2006). Regulons involved in osmotic stress-responsive and cold stress-responsive gene expression in plants. Physiologia Plantarum, 126, 62–71.
Kreps, J. A., Wu, Y., Chang, H. S., Zhu, T., Wang, X., & Harper, J. F. (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology, 130, 2129–2141.
Winfield, M. O., Lu, C., Wilson, I. D., Coghill, J. A., & Edwards, K. J. (2010). Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnology Journal, 8, 749–771.
Zhang, T., Zhao, X., Wang, W., Pan, Y., Huang, L., Liu, X., & Fu, B. (2012). Comparative transcriptome profiling of chilling stress responsiveness in two contrasting rice genotypes. PLoS One, 7(8), e43274.
Tommasini, L., Svensson, J. T., Rodriguez, E. M., Wahid, A., Malatrasi, M., Kato, K., & Close, T. J. (2008). Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Functional & Integrative Genomics, 8(4), 387–405.
William, R. (2006). The association among gene expression responses to nine abiotic stress. Treatments in Arabidopsis Thaliana Genetics, 174, 1811–1824.
Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., et al. (2004). Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal, 37, 914–939.
Rotter, A., Usadel, B., Baebler, S., Stitt, M., & Gruden, K. (2007). Adaptation of the MapMan ontology to biotic stress responses: application in Solanaceous species. Plant Methods, 3, 10.
Song, Y., Chen, Q., Ci, D., & Zhang, D. (2013). Transcriptome profiling reveals differential transcript abundance in response to chilling stress in Populus simonii. Plant Cell Reports, 32(9), 1407–1425.
Tian, D. Q., Pan, X. Y., Yu, Y. M., Wang, W. Y., Zhang, F., Ge, Y. Y., & Liu, X. J. (2013). De novo characterization of the Anthurium transcriptome and analysis of its digital gene expression under cold stress. BMC Genomics, 14(1), 827.
Wang, X. C., Zhao, Q. Y., Ma, C. L., Zhang, Z. H., Cao, H. L., Kong, Y. M., & Yang, Y. J. (2013). Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genomics, 14(1), 415.
Xu, W., Zhang, N., Jiao, Y., Li, R., Xiao, D., & Wang, Z. (2014). The grapevine basic helix-loop-helix (bHLH) transcription factor positively modulates CBF-pathway and confers tolerance to cold-stress in Arabidopsis. Molecular Biology Reports, 41(8), 5329–5342.
Kim, S. A., Ahn, S. Y., Kim, S. H., Han, J. H., & Yun, H. K. (2014). Expression of basic helix-loop-helix transcripts during low temperature treatments in grapevines. The Korean Society of Breeding Science, 2(2), 110–116.
Huang, X. S., Wang, W., Zhang, Q., & Liu, J. H. (2013). A basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiology, 162(2), 1178–1194.
Feng, X. M., Zhao, Q., Zhao, L. L., Qiao, Y., Xie, X. B., Li, H. F., & Hao, Y. J. (2012). The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biology, 12(1), 22.
Wang, Y. J., Zhang, Z. G., He X. J , Zhou, H. L., Wen, Y. X., Dai, J. X., Zhang, J. S., & Chen, S. Y. (2003). A rice transcription factor OsbHLH1 is involved in cold stress response. Theoretical and Applied Genetics, 107, 1402–1409.
Seo, J. S., Joo, J., Kim, M. J., Kim, Y. K., Nahm, B. H., Song, S. I., & Choi, Y. D. (2011). OsbHLH148, a basic helix‐loop‐helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. The Plant Journal, 65(6), 907–921.
Fursova, O. V., Pogorelko, G. V., & Tarasov, V. A. (2009). Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene, 429(1), 98–103.
Peng, H. H., Shan, W., Kuang, J. F., Lu, W. J., & Chen, J. Y. (2013). Molecular characterization of cold-responsive basic helix-loop-helix transcription factors MabHLHs that interact with MaICE1 in banana fruit. Planta, 238(5), 937–953.
Chen, L., Song, Y., Li, S., Zhang, L., Zou, C., & Yu, D. (2012). The role of WRKY transcription factors in plant abiotic stresses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1819(2), 120–128.
Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., & Shinozaki, K. (2002). Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high‐salinity stresses using a full‐length cDNA microarray. The Plant Journal, 31(3), 279–292.
Zhou, Q. Y., Tian, A. G., Zou, H. F., Xie, Z. M., Lei, G., Huang, J., & Chen, S. Y. (2008). Soybean WRKY‐type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnology Journal, 6(5), 486–503.
Mare, C., Mazzucotelli, E., Crosatti, C., Francia, E., & Cattivelli, L. (2004). Hv-WRKY38: a new transcription factor involved in cold-and drought-response in barley. Plant Molecular Biology, 55(3), 399–416.
Ramamoorthy, R., Jiang, S. Y., Kumar, N., Venkatesh, P. N., & Ramachandran, S. (2008). A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant and Cell Physiology, 49(6), 865–879.
Hwang, E. W., Kim, K. A., Park, S. C., Jeong, M. J., Byun, M. O., & Kwon, H. B. (2005). Expression profiles of hot pepper (Capsicum annuum) genes under cold stress conditions. Journal of Biosciences, 30(5), 657–667.
Jiang, Y., Duan, Y., Yin, J., Ye, S., Zhu, J., Zhang, F., & Luo, K. (2014). Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. Journal of Experimental Botany, 65, 6629–6644.
Wang, L., Zhu, W., Fang, L., Sun, X., Su, L., Liang, Z., & Xin, H. (2014). Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biology, 14(1), 103.
Li, L., Yu, Y., Wei, J., Huang, G., Zhang, D., Liu, Y., & Zhang, L. (2013). Homologous HAP5 subunit from Picea wilsonii improved tolerance to salt and decreased sensitivity to ABA in transformed Arabidopsis. Planta, 238(2), 345–356.
Chen, N. Z., Zhang, X. Q., Wei, P. C., Chen, Q. J., Ren, F., Chen, J., & Wang, X. C. (2007). AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. Journal of Biochemistry and Molecular Biology, 40, 1083–1089.
Nelson, D. E., Repetti, P. P., Adams, T. R., Creelman, R. A., Wu, J., Warner, D. C., Anstrom, D. C., Bensen, R. J., Castiglioni, P. P., & Donnarummo, M. G. (2007). Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National academy of Sciences of the United States of America, 104, 16450–16455.
Shi, H., Ye, T., Zhong, B., Liu, X., Jin, R., & Chan, Z. (2014). AtHAP5A modulates freezing stress resistance in Arabidopsis through binding to CCAAT motif of AtXTH21. New Phytologist, 203(2), 554–567.
Nijhawan, A., Jain, M., Tyagi, A. K., & Khurana, J. P. (2008). Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiology, 146(2), 333–350.
Liu, C., Wu, Y., & Wang, X. (2012). bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta, 235(6), 1157–1169.
Tak, H., & Mhatre, M. (2013). Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera. Protoplasma, 250(1), 333–345.
Zhang, L., Zhang, L., Xia, C., Zhao, G., Liu, J., Jia, J., & Kong, X. (2014). A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiologia Plantarum, 153(4), 538–554.
Liao, Y., Zou, H. F., Wei, W., Hao, Y. J., Tian, A. G., Huang, J., & Chen, S. Y. (2008). Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta, 228(2), 225–240.
Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., & Tran, L. S. P. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany, 64(2), 445–458.
Hwang, S. G., Kim, D. S., & Jang, C. S. (2011). Comparative analysis of evolutionary dynamics of genes encoding leucine-rich repeat receptor-like kinase between rice and Arabidopsis. Genetica, 139, 1023–1032.
Marshall, A., Aalen, R. B., Audenaert, D., Beeckman, T., Broadley, M. R., Butenko, M. A., & De Smet, I. (2012). Tackling drought stress: receptor-like kinases present new approaches. The Plant Cell Online, 24(6), 2262–2278.
Dardick, C., Chen, J., Richter, T., Ouyang, S., & Ronald, P. (2007). The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiology, 143, 579–586.
Shiu, S. H., & Bleecker, A. B. (2003). Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiology, 132, 530–543s.
Huang, G. T., Ma, S. L., Bai, L. P., Zhang, L., Ma, H., Jia, P., & Guo, Z. F. (2012). Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39(2), 969–987.
Chinnusamy, V., Schumaker, K., & Zhu, J. K. (2003). Molecular genetic perspectives on cross-talk and specificity in abiotic stress signaling in plants. Journal of Experimental Botany, 55(395), 225–236.
Morrison, D. K. (2012). MAP kinase pathways. Cold Spring Harbor Perspectives in Biology, 4(11), a011254.
Reddy, A. S., Ali, G. S., Celesnik, H., & Day, I. S. (2011). Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell, 23, 2010–2032.
DeFalco, T. A., Bender, K. W., & Snedden, W. A. (2010). Breaking the code: Ca2+ sensors in plant 371 signaling. Biochemistry Journal, 425, 27–40.
Batistic, O., & Kudla, J. (2012). Analysis of calcium signaling pathways in plants. Biochimica et Biophysica Acta (BBA) - General Subjects, 1820(8), 1283–1293.
Santner, A., & Estelle, M. (2009). Recent advances and emerging trends in plant hormone signaling. Nature, 459(7250), 1071–1078.
Peleg, Z., & Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14(3), 290–295.
Narusaka, Y., Nakashima, K., Shinwari, Z. K., Sakuma, Y., Furihata, T., Abe, H., Narusaka, M., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2003). Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant Journal, 34, 137–148.
Jain, M., & Khurana, J. P. (2009). Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS Journal, 276(11), 3148–3162.
Shibasaki, K., Uemura, M., Tsurumi, S., & Rahman, A. (2009). Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. The Plant Cell Online, 21(12), 3823–3838.
Hannah, M. A., Heyer, A. G., & Hincha, D. K. (2005). A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genetics, 1, 179–196.
Chen, Y. F., Etheridge, N., & Schaller, G. E. (2005). Ethylene signal transduction. Annals of Botany, 95(6), 901–915.
Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., & Yang, S. (2012). Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. The Plant Cell Online, 24(6), 2578–2595.
Zhao, M., Liu, W., Xia, X., Wang, T., & Zhang, W. H. (2014). Cold acclimation-induced freezing tolerance of Medicago truncatula seedlings is negatively regulated by ethylene. Physiologia Plantarum, 152(1), 115–129.
Zhao, D., Shen, L., Fan, B., Yu, M., Zheng, Y., Lv, S., & Sheng, J. (2009). Ethylene and cold participate in the regulation of LeCBF1 gene expression in postharvest tomato fruits. FEBS Letters, 583(20), 3329–3334.
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. Journal of Experimental Botany, 64(6), 1755–1767.
Uemura, M., Joseph, R. A., & Steponkus, P. L. (1995). Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiology, 109, 15–30.
Yadav, S. K. (2010). Cold stress tolerance mechanisms in plants. A review. Agronomy for Sustainable Development, 30, 515–527.
Amiri, R. M., Yur’eva, N. O., Shimshilashvili, K. R., Goldenkova-Pavlova, I. V., Pchelkin, V. P., Kuznitsova, E. I., & Nosov, A. M. (2010). Expression of acyl-lipid Δ12-desaturase gene in prokaryotic and eukaryotic cells and its effect on cold stress tolerance of potato. Journal of Integrative Plant Biology, 52(3), 289–297.
Biswal, B., Joshi, P. N., Raval, M. K., & Biswal, U. C. (2011). Photosynthesis, a global sensor of environmental stress in green plants: stress signalling and adaptation. Current Science (Bangalore), 101(1), 47–56.
Koc, I., Filiz, E., & Tombuloglu, H. (2015). Assessment of miRNA expression profile anddifferential expression pattern of target genes in cold-tolerant and cold-sensitive tomato cultivars. Biotechnology & Biotechnological Equipment, doi:10.1080/13102818.2015.1061447
Savitch, L. V., Barker-Astrom, J., Ivanov, A. G., Hurry, V., Oquist, G., et al. (2001). Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma. Planta, 214, 295–303.
Huner, N. P. A., Oquist, G., & Sarhan, F. (1998). Energy balance and acclimation to light and cold. Trends in Plant Science, 3, 224–230.
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Koc, I., Vatansever, R., Ozyigit, I.I. et al. Identification of Differentially Expressed Genes in Chilling-Induced Potato (Solanum tuberosum L.); a Data Analysis Study. Appl Biochem Biotechnol 177, 792–811 (2015). https://doi.org/10.1007/s12010-015-1778-9
- Cold acclimation
- COR genes
- Signal transduction