Journal of Plant Growth Regulation

, Volume 33, Issue 2, pp 460–469 | Cite as

Interaction of Temperature and Light in the Development of Freezing Tolerance in Plants

  • Tibor JandaEmail author
  • Imre Majláth
  • Gabriella Szalai


Freezing tolerance is the result of a wide range of physical and biochemical processes, such as the induction of antifreeze proteins, changes in membrane composition, the accumulation of osmoprotectants, and changes in the redox status, which allow plants to function at low temperatures. Even in frost-tolerant species, a certain period of growth at low but nonfreezing temperatures, known as frost or cold hardening, is required for the development of a high level of frost hardiness. It has long been known that frost hardening at low temperature under low light intensity is much less effective than under normal light conditions; it has also been shown that elevated light intensity at normal temperatures may partly replace the cold-hardening period. Earlier results indicated that cold acclimation reflects a response to a chloroplastic redox signal while the effects of excitation pressure extend beyond photosynthetic acclimation, influencing plant morphology and the expression of certain nuclear genes involved in cold acclimation. Recent results have shown that not only are parameters closely linked to the photosynthetic electron transport processes affected by light during hardening at low temperature, but light may also have an influence on the expression level of several other cold-related genes; several cold-acclimation processes can function efficiently only in the presence of light. The present review provides an overview of mechanisms that may explain how light improves the freezing tolerance of plants during the cold-hardening period.


Chloroplast Cold hardening Excitation Freezing Frost tolerance Photosynthesis Plant hormones Signalling 



This work was supported by OTKA 104963. Thanks to Barbara Harasztos for revising the English.


  1. Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372CrossRefPubMedGoogle Scholar
  2. Apostol S, Szalai G, Sujbert L, Popova LP, Janda T (2006) Non-invasive monitoring of the light-induced cyclic photosynthetic electron flow during cold hardening in wheat leaves. Z Naturforsch C 61:734–740CrossRefPubMedGoogle Scholar
  3. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190CrossRefGoogle Scholar
  4. Boneh U, Biton I, Schwartz A, Ben-Ari G (2012) Characterization of the ABA signal transduction pathway in Vitis vinifera. Plant Sci 187:89–96CrossRefPubMedGoogle Scholar
  5. Boonman A, Prinsen E, Gilmer F, Schurr U, Peeters AJM, Voesenek LACJ, Pons TL (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiol 143:1841–1852PubMedCentralCrossRefPubMedGoogle Scholar
  6. Cansev A, Gulen H, Eris A (2009) Cold-hardiness of olive (Olea europaea L.) cultivars in cold-acclimated and non-acclimated stages: seasonal alteration of antioxidative enzymes and dehydrin-like proteins. J Agric Sci 147:51–61CrossRefGoogle Scholar
  7. Chandler JW (2009) Auxin as compère in plant hormone crosstalk. Planta 231:1–12CrossRefPubMedGoogle Scholar
  8. Chen WQ, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou GZ, Whitham SA, Budworth PR, Tao Y, Xie ZY, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dang JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574PubMedCentralCrossRefPubMedGoogle Scholar
  9. Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, Hwang I (2010) The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev Cell 19:284–295CrossRefPubMedGoogle Scholar
  10. Crosatti C, Rizza F, Badeck FW, Mazzucotelli E, Cattivelli L (2013) Harden the chloroplast to protect the plant. Physiol Plant 147(1):55–63CrossRefPubMedGoogle Scholar
  11. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signalling network. Annu Rev Plant Biol 61:651–679CrossRefPubMedGoogle Scholar
  12. Degenkolbe T, Giavalisco P, Zuther E, Seiwert B, Hincha DK, Dirk K, Willmitzer L (2012) Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. Plant J 72:972–982PubMedGoogle Scholar
  13. Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373CrossRefPubMedGoogle Scholar
  14. Ensminger I, Busch F, Huner NPA (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126:28–44CrossRefGoogle Scholar
  15. Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signalling in seeds and seedlings. Plant Cell 14:515–545Google Scholar
  16. Franklin KA (2009) Light and temperature signal crosstalk in plant development. Curr Opin Plant Biol 12:63–68CrossRefPubMedGoogle Scholar
  17. Franklin KA, Whitelam GC (2007) Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39:1410–1413CrossRefPubMedGoogle Scholar
  18. Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6(11):1746–1751PubMedCentralCrossRefPubMedGoogle Scholar
  19. Gray GR, Chauvin LP, Sarhan F, Huner N (1997) Cold acclimation and freezing tolerance (a complex interaction of light and temperature). Plant Physiol 114:467–474PubMedCentralPubMedGoogle Scholar
  20. Gulick PJ, Drouin S, Yu Z, Danyluk J, Poisson G, Monroy AF, Sarhan F (2005) Transcriptome comparison of winter and spring wheat responding to low temperature. Genome 48:913–923CrossRefPubMedGoogle Scholar
  21. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223CrossRefGoogle Scholar
  22. Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters, and regulatory factors. Plant Mol Biol 49:373–385CrossRefPubMedGoogle Scholar
  23. Hayashi H, Alia, Mustardy L, Deshnium P, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12(1):133–142CrossRefPubMedGoogle Scholar
  24. Holmström KO, Somersalo S, Mandal A, Palva TE, Welin B (2000) Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51(343):177–185CrossRefPubMedGoogle Scholar
  25. Horváth E, Pál M, Szalai G, Páldi E, Janda T (2007a) Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat (Triticum aestivum L.) plants. Biol Plant 51:480–487CrossRefGoogle Scholar
  26. Horváth E, Szalai G, Janda T (2007b) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300CrossRefGoogle Scholar
  27. Howarth CJ, Ougham HJ (1993) Gene expression under temperature stress. New Phytol 125:1–26CrossRefGoogle Scholar
  28. Huner NPA, Williams JP, Maissan EE, Myscich EG, Krol M, Laroche A, Singh J (1989) Low temperature-induced decrease in trans-Δ3-hexadecenoic acid content is correlated with freezing tolerance in cereals. Plant Physiol 89:144–150PubMedCentralCrossRefPubMedGoogle Scholar
  29. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3(6):224–230CrossRefGoogle Scholar
  30. Hurry VM, Huner NP (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol 100(3):1283–1290PubMedCentralCrossRefPubMedGoogle Scholar
  31. Hurry VM, Strand A, Tobiaeson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol 109:697–706PubMedCentralPubMedGoogle Scholar
  32. Janda T, Kissimon J, Szigeti Z, Veisz O, Páldi E (1994) Characterization of cold hardening in wheat using fluorescence induction parameters. J Plant Physiol 143:385–388CrossRefGoogle Scholar
  33. Janda T, Szalai G, Rios-Gonzalez K, Veisz O, Páldi E (2003) Comparative study of frost tolerance and antioxidant activity in cereals. Plant Sci 164:301–306CrossRefGoogle Scholar
  34. Janda T, Szalai G, Leskó K, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674–1682CrossRefPubMedGoogle Scholar
  35. Jeon J, Kim J (2013) Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol 161:408–424PubMedCentralCrossRefPubMedGoogle Scholar
  36. Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku SJ, Cho C, Lee DJ, Lee EJ, Strnad M, Kim J (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23369–23384Google Scholar
  37. Kang HG, Singh KB (2000) Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. Plant J 21:329–339CrossRefPubMedGoogle Scholar
  38. Keren N, Krieger-Liszkay A (2011) Photoinhibition: molecular mechanisms and physiological significance. Physiol Plant 142:1–5CrossRefPubMedGoogle Scholar
  39. Kim HJ, Kim YK, Park JY, Kim J (2002) Light signalling mediated by phytochrome plays an important role in cold-induced gene expression through the C repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J 29:693–704CrossRefPubMedGoogle Scholar
  40. Klíma M, Vítámvás P, Zelenková S, Vyvadilová M, Prášil IT (2012) Dehydrin and proline content in Brassica napus and B. carinata under cold stress at two irradiances. Biol Plant 56:157–161CrossRefGoogle Scholar
  41. Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751CrossRefPubMedGoogle Scholar
  42. Kocsy G, Pál M, Soltész A, Szalai G, Boldizsár Á, Kovács V, Janda T (2011) Low temperature and oxidative stress in cereals. Acta Agron Hung 59:169–189CrossRefGoogle Scholar
  43. Kosová K, Holková L, Prášil IT, Prášilová P, Bradáčová M, Vítámvás P, Čapková V (2008) The expression of dehydrin5 during the development of frost tolerance in barley (Hordeum vulgare). J Plant Physiol 165:1142–1151CrossRefPubMedGoogle Scholar
  44. Kosová K, Prášil IT, Prášilová P, Vítámvás P, Chrpová J (2010) The development of frost tolerance and DHN5 protein accumulation in barley (Hordeum vulgare) doubled haploid lines derived from Atlas68 × Igri cross during cold acclimation. J Plant Physiol 167:343–350CrossRefPubMedGoogle Scholar
  45. Kosová K, Prasil IT, Vitamvas P, Dobrev P, Motyka V, Flokova K, Novak O, Turecková V, Rolcik J, Pesek B, Travnickova A, Gaudinova A, Galiba G, Janda T, Vlasakova E, Prasilova P, 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 169:567–576CrossRefPubMedGoogle Scholar
  46. Kruse O, Hankamer B, Konczak C, Gerle C, Morris E, Radunz A, Schmid GH, Barber J (2000) Phosphatidylglycerol is involved in the dimerization of photosystem II. J Biol Chem 275:6509–6514CrossRefPubMedGoogle Scholar
  47. Lee CM, Thomashow MF (2012) Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:15054–15059PubMedCentralCrossRefPubMedGoogle Scholar
  48. Levitt J (1972) Freezing resistance: types, measurements, and changes. In: Kozlowski TT (ed) Responses of plants to environmental stresses. Academic Press, New York, pp 75–109Google Scholar
  49. Maibam P, Nawkar GM, Park JH, Sahi VP, Lee SY, Kang CH (2013) The influence of light quality, circadian rhythm, and photoperiod on the CBF-mediated freezing tolerance. Int J Mol Sci 14:11527–11543PubMedCentralCrossRefPubMedGoogle Scholar
  50. Majláth I, Szalai G, Soós V, Sebestyén E, Balázs E, Vanková R, Dobrev PI, Tandori J, Janda T (2012) Effect of light on the gene expression and hormonal status of winter and spring wheat plants during cold hardening. Physiol Plant 145:296–314CrossRefPubMedGoogle Scholar
  51. McKown R, Kuroki G, Warren G (1996) Cold responses of Arabidopsis mutants impaired in freezing tolerance. J Exp Bot 47:1919–1925CrossRefGoogle Scholar
  52. Mira-Rodado V, Sweere U, Grefen C, Kunkel T, Fejes E, Nagy F, Schafer E, Harter K (2007) Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis. J Exp Bot 58:2595–2607CrossRefPubMedGoogle Scholar
  53. Muday GK, Rahman A, Binder B (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17:181–195CrossRefPubMedGoogle Scholar
  54. Ndong C, Danyluk J, Huner NPA, Sarhan F (2001) Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure. Plant Mol Biol 45:691–703CrossRefPubMedGoogle Scholar
  55. Ndong C, Danyluk J, Kenneth E, Wilson KE, Tessa Pocock T, Huner NPA, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368–1381PubMedCentralCrossRefPubMedGoogle Scholar
  56. Noctor G (2006) Metabolic signalling in defence and stress: the central role of soluble redox couples. Plant Cell Environ 29:409–425CrossRefPubMedGoogle Scholar
  57. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefPubMedGoogle Scholar
  58. Ntatsi G, Savvas D, Druege U, Schwarz D (2013) Contribution of phytohormones in alleviating the impact of sub-optimal temperature stress on grafted tomato. Sci Hortic 149:28–38CrossRefGoogle Scholar
  59. Pagter M, Lefevre I, Arora R, Hausman JF (2011) Quantitative and qualitative changes in carbohydrates associated with spring deacclimation in contrasting Hydrangea species. Environ Exp Bot 72:358–367CrossRefGoogle Scholar
  60. Pál M, Leskó K, Janda T, Páldi E, Szalai G (2007) Cadmium-induced changes in the membrane lipid composition of maize plants. Cereal Res Commun 35:1631–1642CrossRefGoogle Scholar
  61. Patel D, Franklin KA (2009) Temperature-regulation of plant architecture. Plant Signal Behav 4:577–579PubMedCentralCrossRefPubMedGoogle Scholar
  62. Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35CrossRefPubMedGoogle Scholar
  63. Sasheva P, Szalai G, Janda T, Popova L (2010) Study of the behaviour of antioxidant enzymes in the response to hardening and freezing stress in two wheat (Triticum aestivum L.) varieties. C R Acad Bulg Sci 63:1733–1740Google Scholar
  64. Sheen J, Zhou L, Jang JC (1999) Sugars as signaling molecules. Curr Opin Plant Biol 2:410–418CrossRefPubMedGoogle Scholar
  65. 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. Plant Cell 24:2578–2595PubMedCentralCrossRefPubMedGoogle Scholar
  66. Shinozaki KY, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefPubMedGoogle Scholar
  67. Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8:13PubMedCentralCrossRefPubMedGoogle Scholar
  68. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037CrossRefPubMedGoogle Scholar
  69. Stephenson TJ, McIntyre CL, Collet C, Xue GP (2010) TaNF-YC11, one of the light-upregulated NF-YC members in Triticum aestivum, is co-regulated with photosynthesis-related genes. Funct Integr Genomics 10:265–276CrossRefPubMedGoogle Scholar
  70. Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49:411–426CrossRefPubMedGoogle Scholar
  71. Szalai G, Janda T, Páldi E, Dubacq J-P (2001) Changes in the fatty acid unsaturation after hardening in wheat chromosome substitution lines with different cold tolerance. J Plant Physiol 158:663–666CrossRefGoogle Scholar
  72. Szalai G, Pap M, Janda T (2009a) Light-induced frost tolerance differs in winter and spring wheat plants. J Plant Physiol 166:1826–1831CrossRefPubMedGoogle Scholar
  73. Szalai G, Kellos T, Galiba G, Kocsy G (2009b) Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J Plant Growth Regul 28:66–80CrossRefGoogle Scholar
  74. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599CrossRefPubMedGoogle Scholar
  75. Vítámvás P, Saalbach G, Prášil IT, Čapková V, Opatrná J, Jahoor A (2007) WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J Plant Physiol 164:1197–1207CrossRefPubMedGoogle Scholar
  76. Vítámvás P, Kosová K, Prášilová P, Prášil IT (2010) Accumulation of WCS120 protein in wheat cultivars grown at 9 °C or 17 °C in relation to their winter survival. Plant Breed 129:611–616CrossRefGoogle Scholar
  77. Wang JH, Li SC, Sun M, Huang W, Cao H, Xu F, Zhou NN, Zhang SB (2013) Differences in the stimulation of cyclic electron flow in two tropical ferns under water stress are related to leaf anatomy. Physiol Plant 147:283–295CrossRefPubMedGoogle Scholar
  78. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–400PubMedCentralCrossRefPubMedGoogle Scholar
  79. Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771CrossRefPubMedGoogle Scholar
  80. Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461CrossRefPubMedGoogle Scholar
  81. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(suppl):S165–S183PubMedCentralPubMedGoogle Scholar
  82. Yelenosky G (1979) Accumulation of free proline in citrus leaves during cold hardening of young trees in controlled temperature regimes. Plant Physiol 64:425–427PubMedCentralCrossRefPubMedGoogle Scholar
  83. Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126:1232–1240PubMedCentralCrossRefPubMedGoogle Scholar
  84. Zaltsman A, Ori N, Adam Z (2005) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17:2782–2790PubMedCentralCrossRefPubMedGoogle Scholar
  85. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCentralCrossRefPubMedGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Agricultural Institute, Centre for Agricultural ResearchHungarian Academy of SciencesMartonvásárHungary

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