Skip to main content

Advertisement

Log in

Cold stress tolerance mechanisms in plants. A review

  • Review Article
  • Published:
Agronomy for Sustainable Development Aims and scope Submit manuscript

Abstract

The human population is increasing at an alarming rate, whereas at the same time agricultural productivity is decreasing due to the effect of various environmental problems. In particular, cold stress is a serious threat to the sustainability of crop yields. Indeed, cold stress can lead to major crop losses. Various phenotypic symptoms in response to cold stress include poor germination, stunted seedlings, yellowing of leaves (chlorosis), reduced leaf expansion and wilting, and may lead to death of tissue (necrosis). Cold stress also severely hampers the reproductive development of plants. The major negative effect of cold stress is that it induces severe membrane damage. This damage is largely due to the acute dehydration associated with freezing during cold stress. Cold stress is perceived by the receptor at the cell membrane. Then a signal is transduced to switch on the cold-responsive genes and transcription factors for mediating stress tolerance. Understanding the mechanism of cold stress tolerance and genes involved in the cold stress signaling network is important for crop improvement. Here, I review cold stress tolerance mechanisms in plants. The major points discussed are the following: (1) physiological effects of cold stress, (2) sensing of cold temperatures and signal transduction, and (3) the role of various cold-responsive genes and transcription factors in the mechanism of cold stress tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbasi F., Onodera H., Toki S., Tanaka H., Komatsu S. (2004) OsCDPK13, a calcium dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath, Plant Mol. Biol. 55, 541–552.

    PubMed  CAS  Google Scholar 

  • Agarwal M., Hao Y., Kapoor A., Dong C.H., Fujii H., Zheng X., Zhu J.K. (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance, J. Biol. Chem. 281, 37636–37645.

    PubMed  CAS  Google Scholar 

  • Anderson J.V., Li Q.B., Haskell D.W., Guy C.L. (1994) Structural organization of the spinach endoplasmic reticulum-luninal 70-kilodalton heat shock cognate gene and expression of 70-kilodalton heat shock genes during cold acclimation, Plant Physiol. 104, 1359–1370.

    PubMed  CAS  Google Scholar 

  • Artus N.N., Uemura M., Steponkus P.L., Gilmour S.J., Lin C.T., Thomashow M.F. (1996) Constitutive expression of the cold regulated Arabidopsis thaliana COR 15a gene affects both chloroplast and protoplast freezing tolerance, Proc. Natl Acad. Sci. (USA) 93, 13404–13409.

    CAS  Google Scholar 

  • Baek K.H., Skinner D.Z. (2003) Alteration of antioxidant enzyme gene expression during cold acclimation of near-isogenic wheat lines, Plant Sci. 165, 1221–1227.

    CAS  Google Scholar 

  • Bray E.A. (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana, J. Exp. Bot. 55, 2331–2341.

    PubMed  CAS  Google Scholar 

  • Cheng C., Yun K.Y., Ressom H.W., Mohanty B., Bajic V.B., Jia Y., Yun S.J., de los Reyes B.G. (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice, BMC Genomics 8, 175.

    PubMed  Google Scholar 

  • Chinnusamy V., Ohta M., Kanrar S., Lee B.H., Hong X., Agarwal M., Zhu J.K. (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis, Gene. Dev. 17, 1043–1054.

    PubMed  CAS  Google Scholar 

  • Chinnusamy V., Zhu J., Zhu J.K. (2006) Gene regulation during cold acclimation in plants, Physiol. Plant. 126, 52–61.

    CAS  Google Scholar 

  • Close T.J. (1997) Dehydrins: A commonality in the response of plants to dehydration and low temperature, Physiol. Plantarum 100, 291–296.

    CAS  Google Scholar 

  • Cook D., Fowler S., Fiehn O., Thomashow M.F. (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis, Proc. Natl Acad. Sci. (USA) 101, 15243–15248.

    CAS  Google Scholar 

  • Cushman J.C., Bohnert H.J. (2000) Genome approaches to plant stress tolerance, Curr. Opin. Plant Biol. 3, 117–124.

    PubMed  CAS  Google Scholar 

  • Dai X., Xu Y., Ma Q., Xu W., Wang T., Xue Y., Chong K. (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis, Plant Physiol. 143, 1739–1751.

    PubMed  CAS  Google Scholar 

  • Donson J., Fang Y., Espiritu-Santo G., Xing W., Salazar A., Miyamoto S., Armendarez V., Volkmuth W. (2002) Comprehensive gene expression analysis by transcript profiling, Plant Mol. Biol. 48, 75–97.

    PubMed  CAS  Google Scholar 

  • Dubouzet J.G., Sakuma Y., Ito Y., Kasuga M., Dubouzet E.G., Miura S., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, highaltand cold-responsive gene expression, Plant J. 33, 751–763.

    PubMed  CAS  Google Scholar 

  • Duggan D.J., Bittner M., Chen Y., Meltzer P., Trent J.M. (1999) Expression profiling using cDNA microarrays, Nat. Genet. 21, 10–14.

    PubMed  CAS  Google Scholar 

  • Dure L. (1993) A repeating 11-mer amino acid motif and plant desiccation, Plant J. 3, 363–369.

    PubMed  CAS  Google Scholar 

  • Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S.M.A. (2009) Plant drought stress: effects, mechanisms and management, Agron. Sustain. Dev. 29, 185–212.

    Google Scholar 

  • Fernie A.R., Geigenberger P., Stitt M. (2005) Flux an important, but neglected, component of functional genomics, Curr. Opin. Plant Biol. 8, 174–182.

    PubMed  CAS  Google Scholar 

  • Fitter A.H., Hay R.K.M. (1981) Environmental Physiology of Plants, Academic Press, New York.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Frankow-Lindberg B.E. (2001) Adaptation to winter stress in nine white clover populations: changes in non-structural carbohydrates during exposure to simulated winter conditions and ‘spring’ regrowth potential, Ann. Bot. 88, 745–751.

    CAS  Google Scholar 

  • Ge L.F., Chao D.Y., Shi M., Zhu M.Z., Gao J.P., Lin H.X. (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes, Planta 228, 191–201.

    PubMed  CAS  Google Scholar 

  • Gibbings J.G., Cook B.P., Dufault M.R., Madden S.L., Khuri S., Turnbull C.J., Dunwell J.M. (2003) Global transcript analysis of rice leaf and seed using SAGE technology, Plant Biotechnol. J. 1, 271–285.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Guy C.L. (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism, Annu. Rev. Plant Phys. 41, 187–223.

    CAS  Google Scholar 

  • Hannah M.A., Wiese D., Freund S., Fiehn O., Heyer A.G., Hincha D.K. (2006) Natural genetic variation of freezing tolerance in Arabidopsis, Plant Physiol. 142, 98–112.

    PubMed  CAS  Google Scholar 

  • Hansen J., Beck E. (1994) Seasonal changes in the utilization and turnover of assimilation products in a 8-year-old Scots pine (Pinus sylvestris L.) trees, Trees 8, 172–182.

    Google Scholar 

  • Hansen J., Türk R., Vogg G., Heim R., Beck E. (1997) Conifer carbohydrate physiology: Updating classical views, in: Rennenberg H., Eschrich W., Ziegler H. (Eds.), Trees — Contributions to Modern Tree Physiology, Leiden: Backhuys Publisher, pp. 97–108.

    Google Scholar 

  • Hernández-Nistal J., Dopico B., Labrador, E. (2002) Cold and salt stress regulates the expression and activity of a chickpea cytosolic Cu/Zn superoxide dismutase, Plant Sci. 163, 507–514.

    Google Scholar 

  • Hopkins W.G. (1999) The physiology of plants under stress, in: Introduction to Plant Physiology, 2nd ed., Wiley, New York, pp. 451–475.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hsieh T.H., Lee J.T., Yang P.T., Chiu L.H., Charng Y.Y., Wang Y.C., Chan M.T. (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato, Plant Physiol. 129, 1086–1094.

    PubMed  CAS  Google Scholar 

  • Hu H., You J., Fang Y., Zhu X., Qi Z., Xiong L. (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice, Plant Mol. Biol. 67, 169–181.

    PubMed  CAS  Google Scholar 

  • Ingram J., Bartels D. (1996) The molecular basis of dehydration tolerance in plants, Annu. Rev. Plant Phys. 47, 377–403.

    CAS  Google Scholar 

  • Ito Y., Katsura K., Maruyama K., Taji T., Kobayashi M., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. (2006) Functional analysis of rice DREB 1/CBF-type transcription factors involved in coldresponsive gene expression in transgenic rice, Plant Cell Physiol. 47, 141–153.

    PubMed  CAS  Google Scholar 

  • Jaglo K.R., Kleff S., Amundsen K.L., Zhang X., Haake V., Zhang J.Z., Deits T., Thomashow M.F. (2001) Components of the Arabidopsis C-repeat/dehydration responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species, Plant Physiol. 127, 910–917.

    PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen K.R., Gilmour S.J., Zarka D.G., Schabenberger O., Thomashow M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance, Science 280, 104–106.

    PubMed  CAS  Google Scholar 

  • Jiang Q.W., Kiyoharu O., Ryozo I. (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice, Plant Physiol. 129, 1880–1891.

    Google Scholar 

  • Jones S.J., Riddle D.L., Pouzyrev A.T., Velculescu V.E., Hillier L., Eddy S.R., Stricklin S.L., Baillie D.L., Waterston R., Marra M.A. (2001) Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans, Genome Res. 11, 1346–1352.

    PubMed  CAS  Google Scholar 

  • Kanneganti V., Gupta A.K. (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice, Plant Mol. Biol. 66, 445–462.

    PubMed  CAS  Google Scholar 

  • Kaplan F., Kopka J., Haskell D.W., Zhao W., Schiller K.C., Gatzke N., Sung D.Y., Guy C.L. (2004) Exploring the temperature-stress metabolome of Arabidopsis, Plant Physiol. 136, 4159–4168.

    PubMed  CAS  Google Scholar 

  • Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress inducible transcription factor, Nat. Biotechnol. 17, 287–291.

    PubMed  CAS  Google Scholar 

  • Kasuga M., Miura S., Shinozaki K., Yamaguchi-Shinozaki K. (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible RD29A promoter improved drought and low-temperature stress tolerance in tobacco by gene transfer, Plant Cell Physiol. 45, 346–350.

    PubMed  CAS  Google Scholar 

  • Katagiri T., Takahashi S., Shinozaki K. (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDd, in dehydration-inducible accumulation of phosphatidic acid in stress signaling, Plant J. 26, 595–605.

    PubMed  CAS  Google Scholar 

  • Kim S., An C.S., Hong Y.N., Lee K.W. (2004) Cold-inducible transcription factor, CaCBF, is associated with a homeodomain leucine zipper protein in hot pepper (Capsicum annuum L.), Mol. Cell 18, 300–308.

    CAS  Google Scholar 

  • Komatsu S., Yang G., Khan M., Onodera H., Toki S., Yamaguchi M. (2007) Overexpression of calcium-dependent protein kinase 13 and calreticulin interacting protein 1 confers cold tolerance on rice plants, Mol. Genet. Genomics 277, 713–723.

    PubMed  CAS  Google Scholar 

  • Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E., Scharf K.D. (2007) Complexity of the heat stress response in plants, Curr. Opin. Plant Biol. 10, 310–316.

    PubMed  CAS  Google Scholar 

  • Kovtun Y., Chiu W.L., Tena G., Sheen J. (2000) Functional analysis of oxidative stress activated mitogen-activated protein kinase cascade in plants, Proc. Natl Acad. Sci. (USA) 97, 2940–2945.

    CAS  Google Scholar 

  • Kranz H., Scholz K., Weisshaar B. (2000) c-MYB oncogene-like genes encoding three MYB repeats occur in all major plant lineages, Plant J. 21, 231–235.

    PubMed  CAS  Google Scholar 

  • 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 Physiol. 130, 2129–2141.

    PubMed  CAS  Google Scholar 

  • Krishna P., Sacco M., Cherutti J.F., Hill S. (1995) Cold-induced accumulation of hsp 90 transcripts in Brasscia napus, Plant Physiol. 107, 915–923.

    PubMed  CAS  Google Scholar 

  • Kubien D.S., von Caemmerer S., Furbank R.T., Sage R.F. (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of rubisco, Plant Physiol. 132, 1577–1585.

    PubMed  CAS  Google Scholar 

  • Laloi C., Apel K., Danon A. (2004) Reactive oxygen signalling: the latest news, Curr. Opin. Plant Biol. 7, 323–328.

    PubMed  CAS  Google Scholar 

  • Larkindale J., Hall J.D., Knight M.R., Vierling E. (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance, Plant Physiol. 138, 882–888.

    PubMed  CAS  Google Scholar 

  • Lee B.H., Henderson D.A., Zhu J.K. (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1, Plant Cell 17, 3155–3175.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Levitt J. (1972) Responses of Plants to Environmental Stresses, Academic Press, New York.

    Google Scholar 

  • Li W., Li M., Zhang W., Welti R., Wang X. (2004) The plasma membrane-bound phospholipase Dd enhances freezing tolerance in Arabidopsis thaliana, Nat. Biotechnol. 22, 427–433.

    PubMed  Google Scholar 

  • Liu K., Wang L., Xu Y., Chen N., Ma Q., Li F., Chong K. (2007) Overexpression of OsCOIN, a putative cold inducible zinc finger protein, increased tolerance to chilling, salt and drought, and enhanced proline level in rice, Planta 226, 1007–1016.

    PubMed  CAS  Google Scholar 

  • Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., Shinozaki K. (1998) Two transcription factors, DREBI and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought and low temperature responsive gene expression respectively, in Arabidopsis, Plant Cell 10, 1391–1406.

    PubMed  CAS  Google Scholar 

  • Llorente F., Oliveros J.C., Martinez-Zapater J.M., Salinas J. (2000) A freezing-sensitive mutant of Arabidopsis, frs1, is a new aba3 allele, Planta 211, 648–655.

    PubMed  CAS  Google Scholar 

  • Lorenz W.W., Dean J.F. (2002) SAGE profiling and demonstration of differential gene expression along the axial developmental gradient of lignifying xylem in loblolly pine (Pinus taeda), Tree Physiol. 22, 301–310.

    PubMed  CAS  Google Scholar 

  • Lynch D.V. (1990) Chilling injury in plants: the relevance of membrane lipids, in: Katterman F. (Ed.), Environmental Injury to Plants, Academic Press, New York, pp. 17–34.

    Google Scholar 

  • Mahajan S., Tuteja N. (2005) Cold, salinity and drought stresses: an overview, Arch. Biochem. Biophys. 444, 139–158.

    PubMed  CAS  Google Scholar 

  • Maruyama K., Sakuma Y., Kasuga M., Ito Y., Seki M., Goda H., Shimada Y., Yoshida S., Shinozaki K., Yamaguchi-Shinozaki K. (2004) Identification of cold inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems, Plant J. 38, 982–993.

    PubMed  CAS  Google Scholar 

  • McKersie B.D., Bowley S.R. (1997) Active oxygen and freezing tolerance in transgenic plants, in: Plant Cold Hardiness, Molecular Biology, Biochemistry and Physiology, Plenum, New York, pp. 203–214.

    Google Scholar 

  • Meijer H.J., Munnik T. (2003) Phospholipid-based signaling in plants, Annu. Rev. Plant Biol. 54, 265–306.

    PubMed  CAS  Google Scholar 

  • Meissner R.C., Jin H., Cominelli E., Denekamp M., Fuertes A., Greco R., Kranz H.D., Penfield S., Petroni K., Urzainqui A., Martin C., Paz-Ares J., Smeekens S., Tonelli C., Weisshaar B., Baumann E., Klimyuk V., Marillonnet S., Patel K., Speulman E., Tissier A.F., Bouchez D., Jones J.J., Pereira A., Wisman E., Bevan M. (1999) Function search in a large transcription factor gene family in Arabidopsis: assessing the potential of reverse genetics to identify insertional mutations in R2R3 MYB genes, Plant Cell 11, 1827–1840.

    PubMed  CAS  Google Scholar 

  • Monroy A.F., Castonguay Y., Laberge S., Sarhan F., Vezina L.P., Dhindsa R.S. (1993) A new cold-induced alfalfa gene is associated with enhanced hardening at sub zero temperature, Plant Physiol. 102, 873–879.

    PubMed  CAS  Google Scholar 

  • Morsy M.R., Almutairi A.M., Gibbons J., Yun S.J., de Los Reyes B.G. (2005) The OsLti6 genes encoding low-molecular-weight membrane proteins are differentially expressed in rice cultivars with contrasting sensitivity to low temperature, Gene 344, 171–180.

    PubMed  CAS  Google Scholar 

  • Mukhopadhyay A., Vij S., Tyagi A.K. (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco, Proc. Natl Acad. Sci. (USA) 101, 6309–6314.

    CAS  Google Scholar 

  • Munnik T. (2001) Phosphatidic acid: an emerging plant lipid second messenger, Trends Plant Sci. 6, 227–233.

    PubMed  CAS  Google Scholar 

  • Nakashima K., Tran L.S., Van Nguyen D., Fujita M., Maruyama K., Todaka D., Ito Y., Hayashi N., Shinozaki K., Yamaguchi-Shinozaki K. (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress responsive gene expression in rice, Plant J. 51, 617–630.

    PubMed  CAS  Google Scholar 

  • Nayyar H., Chander K., Kumar S., Bains T. (2005) Glycine betaine mitigates cold stress damage in Chickpea, Agron. Sustain. Dev. 25, 381–388.

    CAS  Google Scholar 

  • Oh S.J., Song S.I., Kim Y.S., Jang H.J., Kim S.Y., Kim M., Kim Y.K., Nahm B.H., Kim J.K. (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth, Plant Physiol. 138, 341–351.

    PubMed  CAS  Google Scholar 

  • Ohnishi T., Sugahara S., Yamada T., Kikuchi K., Yoshiba Y., Hirano H.Y., Tsutsumi N. (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice, Genes Genet. Syst. 80, 135–139.

    PubMed  CAS  Google Scholar 

  • Olien C.R., Smith M.N. (1997) Ice adhesions in relation to freeze stress, Plant Physiol. 60, 499–503.

    Google Scholar 

  • Oono Y., Seki M., Nanjo T., Narusaka M., Fujita M., Satoh R., Satou M., Sakurai T., Ishida J., Akiyama K., Iida K., Maruyama K., Satoh S., Yamaguchi-Shinozaki K., Shinozaki K. (2003) Monitoring expression profiles of Arabidopsis gene expression during rehydration process after dehydration using ca. 7000 full-length cDNA microar ray, Plant J. 34, 868–887.

    PubMed  CAS  Google Scholar 

  • Orvar B.L., Sangwan V., Omann F., Dhindsa R.S. (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity, Plant J. 23, 785–794.

    PubMed  CAS  Google Scholar 

  • Pasquali G., Biricolti S., Locatelli F., Baldoni E., Mattana M. (2008) Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples, Plant Cell Rep. 27, 1677–1686.

    PubMed  CAS  Google Scholar 

  • Patankar S., Munasinghe A., Shoaibi A., Cummings L.M., Wirth D.F. (2001) Serial analysis of gene expression in Plasmodium falciparum reveals the global expression profile of erythrocytic stages and the presence of anti-sense transcripts in the malarial parasite, Mol. Biol. Cell 12, 3114–3125.

    PubMed  CAS  Google Scholar 

  • Pellegrineschi A., Reynolds M., Pacheco M., Brito R.M., Almeraya R., Yamaguchi-Shinozaki K., Hoisington D. (2004) Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions, Genome 47, 493–500.

    PubMed  CAS  Google Scholar 

  • Pramanik M.H., Imai R. (2005) 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. 58, 751–762.

    PubMed  CAS  Google Scholar 

  • Qin F., Sakuma Y., Li J., Liu Q., Li Y-Q., Shinozaki K., Yamaguchi-Shinozaki K. (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L., Plant Cell Physiol. 45, 1042–1052.

    PubMed  CAS  Google Scholar 

  • Quinn P.J. (1985) A lipid phase separation model of low temperature damage to biological membranes, Cryobiology 22, 28–46.

    Google Scholar 

  • Rabbani M.A., Maruyama K., Abe H., Khan M.A., 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.

    PubMed  CAS  Google Scholar 

  • Rosinski J.A., Atchley W.R. (1998) Molecular evolution of the Myb family of transcription factors: evidence for polyphyletic origin, J. Mol. Evol. 46, 74–83.

    PubMed  CAS  Google Scholar 

  • Saijo Y., Hata S., Kyozuka J., Shimamoto K., Izui K. (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants, Plant J. 23, 319–327.

    PubMed  CAS  Google Scholar 

  • Saijo Y., Kinoshita N., Ishiyama K., Hata S., Kyozuka J., Hayakawa T., Nakamura T., Shimamoto K., Yamaya T., Izui K. (2001) A Ca(2+)-dependent protein kinase that endows rice plants with cold- and salt-stress tolerance functions in vascular bundles, Plant Cell Physiol. 42, 1228–1233.

    PubMed  CAS  Google Scholar 

  • Salomoni P., Perrotti D., Martinez R., Franceschi C., Calabretta B. (1997) Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity, Proc. Natl Acad. Sci. (USA) 94, 3296–3301.

    CAS  Google Scholar 

  • Sangwan V., Foulds I., Singh J., Dhindsa R.S. (2001) Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx, Plant J. 27, 1–12.

    PubMed  CAS  Google Scholar 

  • Satoh R., Nakashima K., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. (2002) ACTCAT, a novel cis-acting element for proline- and hypoosmolarity-responsive expression of the ProDH gene encoding proline dehydrogenase in Arabidopsis, Plant Physiol. 130, 709–719.

    PubMed  CAS  Google Scholar 

  • Schwender J., Ohlrogge J., Shachar-Hill Y. (2004) Understanding flux in plant metabolic networks, Curr. Opin. Plant Biol. 7, 309–317.

    PubMed  CAS  Google Scholar 

  • Seki M., Kamei A., Yamaguchi-Shinozaki K., Shinozaki K. (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection, Curr. Opin. Biotech. 14, 194–199.

    PubMed  CAS  Google Scholar 

  • Seki M., Narusaka M., Abe H., Kasuga M., Yamaguchi-Shinozaki K., Carninci P., Hayashizaki Y., Shinozaki K. (2001) Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray, Plant Cell 13, 61–72.

    PubMed  CAS  Google Scholar 

  • Seki M., Narusaka M., Ishida J., Nanjo T., Fujita M., Oono Y., Kamiya A., Nakajima M., Enju A., Sakurai T., Satou M., Akiyama K., Taji T., Yamaguchi-Shinozaki K., Carninci P., Kawai J., Hayashizaki 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, Plant J. 31, 279–292.

    PubMed  CAS  Google Scholar 

  • Seki M., Satou M., Sakurai T., Akiyama K., Iida K., Ishida J., Nakajima M., Enju A., Narusaka M., Fujita M., Oono Y., Kamei A., Yamaguchi-Shinozaki K., Shinozaki K. (2004) RIKEN Arabidopsis fulllength (RAFL) cDNA and its applications for expression profiling under abiotic stress conditions, J. Exp. Bot. 55, 213–223.

    PubMed  CAS  Google Scholar 

  • Senser M., Beck E. (1982) Frost resistance in spruce (Picea abies (L.) Karst): V. Influence of photoperiod and temperature on the membrane lipids of the needles, Z. Pflanzenphysiol. 108, 71–85.

    CAS  Google Scholar 

  • Shima S., Matsui H., Tahara S., Imai R. (2007) Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes, FEBS J. 274, 1192–1201.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shinozaki K., Yamaguchi-Shinozaki K., Seki M. (2003) Regulatory network of gene expression in the drought and cold stress responses, Curr. Opin. Plant Biol. 6, 410–417.

    PubMed  CAS  Google Scholar 

  • Somerville C. (1995) Direct tests of the role of membrane lipid composition in low temperature-induce photoinhibition and chilling sensitivity in plants and cyanobacteria, Proc. Natl Acad. Sci. (USA) 92, 6215–6218.

    CAS  Google Scholar 

  • Steponkus P.L. (1984) Role of the plasma membrane in freezing injury and cold acclimation, Ann. Rev. Plant Physiol. 35, 543–584.

    CAS  Google Scholar 

  • Steponkus P.L., Uemura M., Webb M.S. (1993) A contrast of the cryostability of the plasma membrane of winter rye and spring oat-two species that widely differ in their freezing tolerance and plasma membrane lipid composition, in: Steponkus P.L. (Ed.), Advances in Low-Temperature Biology, Vol. 2, JAI Press, London, pp. 211–312.

    Google Scholar 

  • Stockinge E.J., Gilmour S.J., Thomashow M.F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcription activator that binds to the C repeat/ DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit, Proc. Natl Acad. Sci. (USA) 94, 1035–1040.

    Google Scholar 

  • Stracke R., Werber M., Weisshaar B. (2001) The R2R3-MYB gene family in Arabidopsis thaliana, Curr. Opin. Plant Biol. 4, 447–456.

    PubMed  CAS  Google Scholar 

  • Suzuki K., Nagasuga K., Okada M. (2008) The chilling injury induced by high root temperature in the leaves of rice seedlings, Plant Cell Physiol. 49, 433–442.

    PubMed  CAS  Google Scholar 

  • Tao D.L., Öquist G., Wingsle G.G. (1998) Active oxygen scavengers during cold acclimation of scots pine seedlings in relation to freezing tolerance, Cryobiology 37, 38–45.

    PubMed  CAS  Google Scholar 

  • Teige M., Scheikl E., Eulgem T., Doczi R., Ichimura K., Shinozaki K., Dangl J.L., Hirt H. (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis, Mol. Cell 15, 141–152.

    PubMed  CAS  Google Scholar 

  • Tester M., Bacic A. (2005) Abiotic stress tolerance in grasses. From model plants to crop plants, Plant Physiol. 137, 791–793.

    PubMed  CAS  Google Scholar 

  • Testerink C., Munnik T. (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants, Trends Plant Sci. 10, 368–375.

    PubMed  CAS  Google Scholar 

  • Thomashow M.F. (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms, Annu. Rev. Plant Phys. 50, 571–599.

    CAS  Google Scholar 

  • Tuteja R., Tuteja N. (2004) Serial analysis of gene expression (SAGE): unraveling the bioinformatics tools, Bioessays 26, 916–922.

    PubMed  CAS  Google Scholar 

  • Uemura M., Steponkus P.L. (1997) Effect of cold acclimation on membrane lipid composition and freeze induced membrane destabilization, in: Plant Cold Hardiness, Molecular Biology, Biochemistry and Physiology, Plenum, New York, pp. 171–79.

    Google Scholar 

  • Vannini C., Locatelli F., Bracale M., Magnani E., Marsoni M., Osnato M., Mattana M., Baldoni E., Coraggio I. (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants, Plant J. 37, 115–127.

    PubMed  CAS  Google Scholar 

  • Vaultier M.N., Cantrel C., Vergnolle C., Justin A.M., Demandre C., Benhassaine-Kesri G., Çiçek 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.

    PubMed  CAS  Google Scholar 

  • Velculescu V.E., Zhang L., Vogelstein B., Kinzler K.W. (1995) Serial analysis of gene expression, Science 270, 484–487.

    PubMed  CAS  Google Scholar 

  • Velculescu V.E., Zhang L., Zhou W., Vogelstein J., Basrai M.A., Bassett D.E., Hieter P., Vogelstein B., Kinzler K.W. (1997) Characterization of the yeast transcriptome, Cell 88, 243–251.

    PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

  • Verslues P.E., Zhu J.K. (2005) Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress, Biochem. Soc. T. 33, 375–379.

    CAS  Google Scholar 

  • Vinocur B., Altman A. (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations, Curr. Opin. Biotechnol. 16, 123–132.

    PubMed  CAS  Google Scholar 

  • Viswanathan C., Zhu J.K. (2002) Molecular genetic analysis of cold-regulated gene transcription, Philos. T. Roy. Soc. B 357, 877–886.

    CAS  Google Scholar 

  • Vogel J.T., Zarka D.G., Van Buskirk H.A., Fowler S.G., Thomashow M.F. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis, Plant J. 41, 195–211.

    PubMed  CAS  Google Scholar 

  • Wan B., Lin Y., Mou T. (2007) Expression of rice Ca(2+)-dependent protein kinases (CDPKs) genes under different environmental stresses, FEBS Lett. 581, 1179–1189.

    PubMed  CAS  Google Scholar 

  • Wang L., Cai H., Bai X., Li L.W., Li Y., Zhu Y.M. (2008) Cultivation of transgenic rice plants with OsCDPK7 gene and its salt tolerance, Yi Chuan 30, 1051–1055.

    PubMed  Google Scholar 

  • 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, Theor. Appl. Genet. 107, 1402–1409.

    PubMed  CAS  Google Scholar 

  • Welti R., Li W., Li M., Sang Y., Biesiada H., Zhou H.E., Rajashekar C.B., Williams T.D., Wang X. (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase Da in freezing induced lipid changes in Arabidopsis, J. Biol. Chem. 277, 31994–32002.

    PubMed  CAS  Google Scholar 

  • Williams M.E., Torabinejad J., Cohick E., Parker K., Drake E.J., Thompson J.E., Hortter M., DeWald D.B. (2005) Mutations in the Arabidopsis phosphoinositide phosphatase gene SAC9 lead to over-accumulation of PtdIns(4,5)P2 and constitutive expression of the stress-response pathway, Plant Physiol. 138, 686–700.

    PubMed  CAS  Google Scholar 

  • Williams W.P. (1990) Cold-induced lipid phase transitions, Philos.T. Roy. Soc. B 326, 555–570.

    CAS  Google Scholar 

  • Xiang Y., Huang Y., Xiong L. (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement, Plant Physiol. 144, 1416–1428.

    PubMed  CAS  Google Scholar 

  • Xiong L., Yang Y. (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase, Plant Cell 15, 745–759.

    PubMed  CAS  Google Scholar 

  • Xiong L., Ishitani M., Lee H., Zhu J.K. (2001) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stressand osmotic stress-responsive gene expression, Plant Cell 13, 2063–2083.

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K., Shinozaki K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low temperature, or high-salt stress, Plant Cell 6, 251–264.

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K., Shinozaki K. (2005) Organization of cis-acting regulatory elements in osmotic- and coldstress-responsive promoters, Trends Plant Sci. 10, 88–94.

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K., Shinozaki K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses, Annu. Rev. Plant Biol. 57, 781–803.

    PubMed  CAS  Google Scholar 

  • Yanhui C., Xiaoyuan Y., Kun H., Meihua L., Jigang L., Zhaofeng G., Zhiqiang L., Yunfei Z., Xiaoxiao W., Xiaoming Q., Yunping S., Li Z., Xiaohui D., Jingchu L., Xing-Wang D., Zhangliang C., Hongya G., Li-Jia Q. (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family, Plant Mol. Biol. 60, 107–124.

    PubMed  Google Scholar 

  • Zhang J.Z., Creelman R.A., Zhu J.K. (2004) From laboratory to field. Using information from Arabidopsis to engineer salt, cold, and drought tolerance in crops, Plant Physiol. 135, 615–621.

    PubMed  CAS  Google Scholar 

  • Zhang W., Wang C., Qin C., Wood T., Olafsdottir G., Welti R., Wang X. (2003) The oleate-stimulated phospholipase D, PLDd, and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis, Plant Cell 15, 2285–2295.

    PubMed  CAS  Google Scholar 

  • Zhang W., Yu L., Zhang Y., Wang X. (2005) Phospholipase D in the signaling networks of plant response to abscisic acid and reactive oxygen species, Biochim. Biophys. Acta 1736, 1–9.

    PubMed  CAS  Google Scholar 

  • Zhu J., Dong C.H., Zhu J.K. (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation, Curr. Opin. Plant Biol. 10, 290–295.

    PubMed  CAS  Google Scholar 

  • Zhu J., Verslues P.E., Zheng X., Lee B.H., Zhan X., Manabe Y., Sokolchik I., Zhu Y., Dong C.H., Zhu J.K., Hasegawa P.M., Bressan R.A. (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants, Proc. Natl Acad. Sci. (USA) 102, 9966–9971.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sudesh Kumar Yadav.

About this article

Cite this article

Yadav, S.K. Cold stress tolerance mechanisms in plants. A review. Agron. Sustain. Dev. 30, 515–527 (2010). https://doi.org/10.1051/agro/2009050

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1051/agro/2009050

Navigation