Advertisement

What Can Small Molecules Tell Us About Cold Stress Tolerance in Plants?

  • Valentina Longo
  • Mohsen Janmohammadi
  • Lello Zolla
  • Sara RinalducciEmail author
Chapter

Abstract

Plants display a wide capacity range to survive cold and freezing conditions. Indeed, they are able to sense low, non-freezing temperatures and activate processes that lead to an increase in freezing tolerance, a phenomenon known as cold acclimation (CA). Metabolome analysis not only improves the recognition of the complex interactive nature of plant metabolic networks and their responses to environmental changes but also provides valuable information about plant abiotic stress resistance. Metabolomics is still an evolving field and has not reached adequate development, routine and coverage, such as other “omics” technologies. Volatilomics, a recently born “omics” science which allows to analyse the volatile component of the metabolome, has received considerable attention in abiotic stress studies. However, the integration of “omics” technologies is faced with some limitations, and, subsequently, of about 5000 primary and secondary metabolites that are present in a single plant metabolome, only a small portion has been identified. The main metabolome changes during cold stress include the production of osmoprotecting metabolites, which are involved in the regulation of cellular water relations and the reduction of cellular dehydration. Furthermore, they participate in the remodelling of membrane lipids and maintaining membrane integrity and energy sources. Cold-responsive metabolites have cryoprotective and scavenging activities and possibly also act as stabilisers of proteins and enzymes or as regulators of gene expression. Such cold-responsive metabolites particularly include soluble sugars, amino acids, betaines, organic acids, polyols, polyamines and lipids. Altogether, the accumulation of these functional metabolites is an important strategy for increasing plant survival under freezing temperatures. The analysis of metabolome dynamics in overwintering plants during the different stages of CA and plant development may provide valuable information for the improvement of cold tolerance in breeding processes. Interestingly, the majority of cold-responsive metabolites are also induced by other abiotic stresses, such as drought and salinity. In this chapter, we discuss the effects of cold stress on the metabolome and the roles of some functional metabolites during CA and overwintering.

Keywords

Compatible solutes Cold tolerance Cold-responsive metabolites Proline Winter survival 

References

  1. Abavisani A, Khorshidi M, Sherafatmandjour A (2013) Interaction between cold stress and polyamine on antioxidant properties in dragonhead. Int J Agric Crop Sci 5(21):2555Google Scholar
  2. Abeynayake SW, Etzerodt TP, Jonavičienė K, Byrne S, AspT BB (2015) Fructan metabolism and changes in fructan composition during cold acclimation in perennial ryegrass. Front Plant Sci 6:329PubMedPubMedCentralCrossRefGoogle Scholar
  3. Achyuthan KE, Harper JC, Manginell RP, Moorman MW (2017) Volatile metabolites emission by in vivo microalgae-an overlooked opportunity? Meta 31(3):7Google Scholar
  4. Adam S, Murthy SDS (2014) Effect of cold stress on photosynthesis of plants and possible protection mechanisms. In: Approaches to plant stress and their management. Springer, New Delhi, pp 219–226Google Scholar
  5. Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180(1):31–38PubMedCrossRefPubMedCentralGoogle Scholar
  6. Aretz I, Meierhofer D (2016) Advantages and pitfalls of mass spectrometry based metabolome profiling in systems biology. Int J Mol Sci 17(5):632PubMedCentralCrossRefGoogle Scholar
  7. Ashraf M, Foolad M (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216CrossRefGoogle Scholar
  8. Awasthi R, Bhandari K, Nayyar H (2015) Temperature stress and redox homeostasis in agricultural crops. Front Environ Sci 3:11CrossRefGoogle Scholar
  9. Baek KH, Skinner DZ (2012) Production of reactive oxygen species by freezing stress and the protective roles of antioxidant enzymes in plants. J Agric Chem Environ 1(1):34–40Google Scholar
  10. Baumann K (2017) Stress responses: membrane-to-nucleus signals modulate plant cold tolerance. Nat Rev Mol Cell Biol 18(5):276PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bhandari K, Nayyar H (2014) Low temperature stress in plants: an overview of roles of cryoprotectants in defense. In: Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 193–265CrossRefGoogle Scholar
  12. Bhatnagar-Mathur P, Vadez V, Kiran K, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27:411–424PubMedCrossRefPubMedCentralGoogle Scholar
  13. Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AG, Huner NPA, Corcuera LJ (2007) Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot 58(13):3581–3590PubMedCrossRefPubMedCentralGoogle Scholar
  14. Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytol 175(2):244–254PubMedCrossRefPubMedCentralGoogle Scholar
  15. Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci 108(39):16475–16480PubMedCrossRefPubMedCentralGoogle Scholar
  16. Chen TH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13(9):499–505PubMedCrossRefPubMedCentralGoogle Scholar
  17. Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126(1):52–61CrossRefGoogle Scholar
  18. Colton-Gagnon K, Ali-Benali MA, Mayer BF, DionneR BA, Do Carmo S, Charron JB (2014) Comparative analysis of the cold acclimation and freezing tolerance capacities of seven diploid Brachypodium distachyon accessions. Ann Bot 113(4):681–693PubMedCrossRefPubMedCentralGoogle Scholar
  19. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci U S A 101(42):15243–15248PubMedPubMedCentralCrossRefGoogle Scholar
  20. Copolovici L, Kännaste A, Pazouki L, Niinemets U (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169(7):664–672PubMedCrossRefPubMedCentralGoogle Scholar
  21. Cuevas JC, López-Cobollo R, Alcázar R, Zarza X, Koncz C, Altabella T, Salinas J, Tiburcio AF, Ferrando A (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148(2):1094–1105PubMedPubMedCentralCrossRefGoogle Scholar
  22. D’Agostino L, di Pietro M, Di Luccia A (2005) Nuclear aggregates of polyamines are supramolecular structures that play a crucial role in genomic DNA protection and conformation. FEBS J 272(15):3777–3787PubMedCrossRefPubMedCentralGoogle Scholar
  23. Dai F, Huang Y, Zhou M, Zhang G (2009) The influence of cold acclimation on antioxidative enzymes and antioxidants in sensitive and tolerant barley cultivars. Biol Plant 53(2):257–262CrossRefGoogle Scholar
  24. de Campos MKF, de Carvalho K, de Souza FS, Marur CJ, Pereira LFP, Bespalhok Filho JC, Vieira LGE (2011) Drought tolerance and antioxidant enzymatic activity in transgenic ‘Swingle’citrumelo plants over-accumulating proline. Environ Exp Bot 72(2):242–250CrossRefGoogle Scholar
  25. De Luca V, St Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 5(4):168–173PubMedCrossRefPubMedCentralGoogle Scholar
  26. Degenkolbe T, Giavalisco P, Zuther E, Seiwert B, Hincha DK, Willmitzer L (2012) Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. Plant J 72(6):972–982PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dicke M, Loreto F (2010) Induced plant volatiles: from genes to climate change. Trends Plant Sci 15(3):115–117PubMedCrossRefPubMedCentralGoogle Scholar
  28. Dionne J, Castonguay Y, Nadeau P, Desjardins Y (2001) Amino acid and protein changes during cold acclimation of green-type annual bluegrass (L,) ecotypes. Crop Sci 41(6):1862–1870CrossRefGoogle Scholar
  29. dos Reis SP, Lima AM, de Souza CRB (2012) Recent molecular advances on downstream plant responses to abiotic stress. Int J Mol Sci 13(7):8628–8647PubMedPubMedCentralCrossRefGoogle Scholar
  30. Du YC, Nose A (2002) Effects of chilling temperature on the activity of enzymes of sucrose synthesis and the accumulation of saccharides in leaves of three sugarcane cultivars differing in cold sensitivity. Photosynthetica 40(3):389–395CrossRefGoogle Scholar
  31. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  32. Eastmond PJ, Van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JD, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1 which catalyses the first step in trehalose synthesis is essential for Arabidopsis embryo maturation. Plant J 29(2):225–235PubMedCrossRefGoogle Scholar
  33. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13(4):17R–27RPubMedCrossRefGoogle Scholar
  34. Ells TC, Hansen LT (2011) Increased thermal and osmotic stress resistance in Listeria monocytogenes 568 grown in the presence of trehalose due to inactivation of the phosphotrehalase-encoding gene treA. Appl Environ Microbiol 77(19):6841–6851PubMedPubMedCentralCrossRefGoogle Scholar
  35. Ensminger I, Busch F, Huner N (2006) Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol Plant 126(1):28–44CrossRefGoogle Scholar
  36. Ershadi A, Karimi R, Mahdei KN (2016) Freezing tolerance and its relationship with soluble carbohydrates proline and water content in 12 grapevine cultivars. Acta Physiol Plant 38(1):2CrossRefGoogle Scholar
  37. Fowler DB, Limin AE (2004) Interactions among factors regulating phenological development and acclimation rate determine low-temperature tolerance in wheat. Ann Bot 94(5):717–724PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fowler DB, Byrns BM, Greer KJ (2014) Overwinter low-temperature responses of cereals: analyses and simulation. Crop Sci 54(6):2395–2405CrossRefGoogle Scholar
  39. Fowler DB (2008) Cold acclimation threshold induction temperatures in cereals. Crop Sci 48:1147–1154CrossRefGoogle Scholar
  40. Fujikawa S (2016) Plant responses to freezing. In eLS, Wiley, Ltd (Ed.), ChichesterGoogle Scholar
  41. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5(1):26–33PubMedPubMedCentralCrossRefGoogle Scholar
  42. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124(4):1854–1865PubMedPubMedCentralCrossRefGoogle Scholar
  43. Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6(11):1746–1751PubMedPubMedCentralCrossRefGoogle Scholar
  44. Guan X (2014) Physiology of cold acclimation and deacclimation responses of cool-season grasses: Carbon and hormone metabolism, Doctoral dissertation, University of Massachusetts Amherst. 174Google Scholar
  45. Guo WJ, Nagy R, Chen HY, Pfrunder S, Yu YC, Santelia D, Martinoia E (2014) SWEET17 a facilitative transporter mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol 164(2):777–789PubMedCrossRefGoogle Scholar
  46. Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiologiae Plantarum 35(7):2015–2036CrossRefGoogle Scholar
  47. Gusta LV, Trischuk R, Weiser CJ (2005) Plant cold acclimation: the role of abscisic acid. J Plant Growth Regul 24(4):308–318CrossRefGoogle Scholar
  48. Hakeem KR, Rehman RU, Tahir I (2014) Plant signaling: understanding the molecular crosstalk. Springer, New DelhiGoogle Scholar
  49. Hall R, Beale M, Fiehn O, Hardy N, Sumner L, Bino R (2002) Plant metabolomics the missing link in functional genomics strategies. Plant Cell 14(7):1437–1440PubMedPubMedCentralCrossRefGoogle Scholar
  50. Han H, Gao S, Li B, Dong XC, Feng HL, Meng QW (2010) Overexpression of violaxanthin de-epoxidase gene alleviates photoinhibition of PSII and PSI in tomato during high light and chilling stress. J Plant Physiol 167(3):176–183PubMedCrossRefGoogle Scholar
  51. Hannah MA, Heyer AG, Hincha DK (2005) A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1(2):e26PubMedPubMedCentralCrossRefGoogle Scholar
  52. Harley PC (2013) The roles of Stomatal conductance and compound volatility in controlling the emission of volatile organic compounds from leaves. In: Niinemets Ü, Monson R (eds) Biology controls and models of tree volatile organic compound emissions, tree physiology, vol 5. Springer, DordrechtGoogle Scholar
  53. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7(11):1456–1466PubMedPubMedCentralCrossRefGoogle Scholar
  54. Heldt HW, Piechulla B (2010) Plant biochemistry. Academic Press, LondonGoogle Scholar
  55. Herman EM, Rotter K, Premakumar R, Elwinger G, Bae R, Ehler-King L, Chen S, Livingston DP III (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(14):3601–3618PubMedCrossRefPubMedCentralGoogle Scholar
  56. Hincha DK, Hellwege EM, Heyer AG, Crowe JH (2000) Plant fructans stabilize phosphatidylcholine liposomes during freeze-drying. Eur J Biochem 267(2):535–540PubMedCrossRefPubMedCentralGoogle Scholar
  57. Holzinger R, Sandoval-Soto L, Rottenberger S, Crutzen PJ, Kesselmeier J (2000) Emissions of volatile organic compounds from Quercus ilex L, measured by proton-transfer-reaction mass spectrometry under different environmental conditions. J Geophys Res 105:20573–20579CrossRefGoogle Scholar
  58. Hong J, Yang L, Zhang D, Shi J (2016) Plant metabolomics: an indispensable system biology tool for plant science. Int J Mol Sci 17(6):767PubMedCentralCrossRefGoogle Scholar
  59. Hosseini M, Maali-Amiri R, Mahfoozi S, Fowler DB, Mohammadi R (2016) Developmental regulation of metabolites and low temperature tolerance in lines of crosses between spring and winter wheat. Acta Physiol Plant 38(4):87–98CrossRefGoogle Scholar
  60. Huner NP, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3(6):224–230CrossRefGoogle Scholar
  61. Hurry VM, Strand A, Tobiaeson M, Gardestrom P, Oquist 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(2):697–706PubMedPubMedCentralCrossRefGoogle Scholar
  62. Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Integr Plant Biol 50(10):1223–1229PubMedCrossRefGoogle Scholar
  63. Ivanov AG, Krol M, Sveshnikov D, Malmberg G, Gardeström P, Hurry V, Oquist G, Huner NP (2006) Characterization of the photosynthetic apparatus in cortical bark chlorenchyma of Scots pine. Planta 223(6):1165–1177PubMedCrossRefPubMedCentralGoogle Scholar
  64. Janmohammadi M (2010) Study of interrelationship between vegetative/reproductive transition stage and cold induced proteins expression using proteomics analysis in wheat grown under field conditions. P.hD. University of Tehran Faculty of Agricultural Sciences and Engineering. Tehran 236 pp.Google Scholar
  65. Janmohammadi M (2012) Metabolomic analysis of low temperature responses in plants. Curr Opin Agric 1(1):1–6Google Scholar
  66. Janmohammadi M, Enayati V, Sabaghnia N (2012a) Impact of cold acclimation, de-acclimation and re-acclimation on carbohydrate content and antioxidant enzyme activities in spring and winter wheat. Icel Agric Sci 25:3–11Google Scholar
  67. Janmohammadi M, Mahfoozi S, Tvakkol-Afshari R (2012b) Influence of vegetative/reproductive transition on proline and protein accumulation and expression of freezing tolerance in wheat cultivars grown in temperate and cold climates. Agric For 58(3):67–84Google Scholar
  68. Janmohammadi M, Mahfoozi S (2013) Regulatory network of gene expression during the development of frost tolerance in plants. Curr Opin Agric 2(1):11–19Google Scholar
  69. Janmohammadi M (2014) Identification of leaf proteins differentially accumulated during the overwintering in frost-tolerant winter wheat. Curr Opin Agric 3(1):26–29Google Scholar
  70. Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: changes at the protein level. Phytochemistry 117:76–89PubMedPubMedCentralCrossRefGoogle Scholar
  71. Johnson CH, Gonzalez FJ (2012) Challenges and opportunities of metabolomics. J Cell Physiol 227:2975–2981PubMedCrossRefPubMedCentralGoogle Scholar
  72. Kader DZA, Saleh AA, Elmeleigy SA, Dosoky NS (2011) Chilling-induced oxidative stress and polyamines regulatory role in two wheat varieties. J Taibah Univ Sci 5:14–24CrossRefGoogle Scholar
  73. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis betaamylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44:730–743PubMedCrossRefPubMedCentralGoogle Scholar
  74. Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50(6):967–981PubMedCrossRefPubMedCentralGoogle Scholar
  75. Karakas B (2001) The role of sorbitol synthesis in photosynthesis of peach (Prunus persica). Doctoral dissertation uga. Athens GeorgiaGoogle Scholar
  76. Karimi R, Ershadi A (2015) Role of exogenous abscisic acid in adapting of ‘Sultana’ grapevine to low-temperature stress. Acta Physiol Plant 37(8):1–11CrossRefGoogle Scholar
  77. Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45(6):712–722CrossRefGoogle Scholar
  78. Kazemi-Shahandashti SS, Maali-Amiri R (2018) Global insights of protein responses to cold stress in plants: signaling, defence, and degradation. J Plant Physiol 226:123–135PubMedCrossRefPubMedCentralGoogle Scholar
  79. Kishitani S, Watanabe K, Yasuda S, Arakawa K, Takabe T (1994) Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants. Plant Cell Environ 17(1):89–95CrossRefGoogle Scholar
  80. Kishor K, Polavarapu B, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37(2):300–311CrossRefGoogle Scholar
  81. Klemens PA, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Chardon F, Krapp A, Neuhaus HE (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination growth and stress tolerance in Arabidopsis. Plant Physiol 163(3):1338–1352PubMedPubMedCentralCrossRefGoogle Scholar
  82. Koike M, Okamoto T, Tsuda S, Imai R (2002) A novel plant defensin-like gene of winter wheat is specifically induced during cold acclimation. Biochem Biophys Res Commun 298(1):46–53PubMedCrossRefPubMedCentralGoogle Scholar
  83. Korn M, Peterek S, Mock HP, Heyer AG, Hincha DK (2008) Heterosis in the freezing tolerance and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance. Plant Cell Environ 31(6):813–827PubMedPubMedCentralCrossRefGoogle Scholar
  84. Kovács Z, Simon-Sarkadi L, Vashegyi I, Kocsy G (2012) Different accumulation of free amino acids during short-and long-term osmotic stress in wheat. Sci World J 2012:216521CrossRefGoogle Scholar
  85. Krasensky J, Jonak C (2012) Drought salt and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63(4):1593–1608PubMedPubMedCentralCrossRefGoogle Scholar
  86. Kreuzwieser J, Ku¨hnemann F, Martis A, Urban W, Rennenberg H (2000) Diurnal pattern of acetaldehyde emission by flooded poplar trees. Physiol Plant 108:79–86CrossRefGoogle Scholar
  87. Kuehnbaum NL, Britz-McKibbin P (2013) New advances in separation science for metabolomics: resolving chemical diversity in a post-genomic era. Chem Rev 113:2437–2468PubMedCrossRefPubMedCentralGoogle Scholar
  88. Kumar S, Malik J, Thakur P, Kaistha S, Sharma KD, Upadhyaya HD, Berger JD, Nayyar H (2011) Growth and metabolic responses of contrasting chickpea (Cicer arietinum L.) genotypes to chilling stress at reproductive phase. Acta Physiol Plant 33(3):779–787CrossRefGoogle Scholar
  89. Kurepin LV, Ivanov AG, Zaman M, Pharis RP, Allakhverdiev SI, Hurry V, Hüner NP (2015) Stress-related hormones and glycinebetaine interplay in protection of photosynthesis under abiotic stress conditions. Photosynth Res 126(2–3):221–235PubMedCrossRefPubMedCentralGoogle Scholar
  90. Kuzuyama T, Shimizu T, Takahashi S, Seto H (1998) Fosmidomycin a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett 39:7913–7916CrossRefGoogle Scholar
  91. Lai MC, Wang CC, Chuang MJ, Wu YC, Lee YC (2006) Effects of substrate and potassium on the betaine-synthesizing enzyme glycine sarcosine dimethylglycine N-methyltransferase from a halophilic methanoarchaeon Methanohalophilus portucalensis. Res Microbiol 157(10):948–955PubMedCrossRefPubMedCentralGoogle Scholar
  92. Le MQ, Engelsberger WR, Hincha DK (2008) Natural genetic variation in acclimation capacity at sub-zero temperatures after cold acclimation at 4 C in different Arabidopsis thaliana accessions. Cryobiology 57(2):104–112PubMedCrossRefPubMedCentralGoogle Scholar
  93. 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 109(37):15054–15059PubMedCrossRefPubMedCentralGoogle Scholar
  94. Li C, Junttila O, Heino P, Palva ET (2003) Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol 23:481–487PubMedCrossRefPubMedCentralGoogle Scholar
  95. Li C, Puhakainen T, Welling A, Viherä-Aarnio A, Ernstsen A, Junttila O, Heino P, Palva ET (2002) Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes. Physiol Plant 116:478–488CrossRefGoogle Scholar
  96. Li T, Xu SL, Oses-Prieto JA, Putil S, Xu P, Wang RJ, Li KH, Maltby DA, An LH, Burlingame AL, Deng ZP, Wang ZY (2011) Proteomics analysis reveals post-translational mechanisms for cold induced metabolic changes in Arabidopsis. Mol Plant 4:361–374PubMedPubMedCentralCrossRefGoogle Scholar
  97. Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19(9):998–1011PubMedPubMedCentralCrossRefGoogle Scholar
  98. Lindberg S, Kader MA, Yemelyanov V (2012) Calcium signalling in plant cells under environmental stress. In: Environmental adaptations and stress tolerance of plants in the era of climate change. Springer, New York, pp 325–360CrossRefGoogle Scholar
  99. Liu JH, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126CrossRefGoogle Scholar
  100. Liu W, Yu K, He T, Li F, Zhang D, Liu J (2013) The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. Sci World J 2013:658793Google Scholar
  101. Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:13Google Scholar
  102. Liu W, Su J, Li S, Lang X, Huang X (2018) Non-structural carbohydrates regulated by season and species in the subtropical monsoon broad-leaved evergreen forest of Yunnan Province, China. Sci Rep 8(1):1083Google Scholar
  103. Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29:1820–1828PubMedCrossRefPubMedCentralGoogle Scholar
  104. Ma Y, Dai X, Xu Y, Luo W, Zheng X, Zeng D, Pan Y, Lin X, Liu H, Zhang D, Xiao J, Guo X, Xu S, Niu Y, Jin J, Zhang H, Xu X, Li L, Wang W, Qian Q, Ge S, Chong K (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221PubMedPubMedCentralCrossRefGoogle Scholar
  105. Ma Y, Wang Q, Gao X, Zhang Y (2017) Biosynthesis and uptake of glycine betaine as cold-stress response to low temperature in fish pathogen Vibrio anguillarum. J Microbiol 55(1):44–55PubMedCrossRefPubMedCentralGoogle Scholar
  106. Maeda H, Song W, Sage TL, DellaPenna D (2006) Tocopherols play a crucial role in low-temperature adaptation and phloem loading in Arabidopsis. Plant Cell 18(10):2710–2732PubMedPubMedCentralCrossRefGoogle Scholar
  107. Maffei ME (2010) Sites of synthesis biochemistry and functional role of plant volatiles. S Afr J Bot 76:612–631CrossRefGoogle Scholar
  108. Maffei ME, Gertsch J, Appendino G (2011) Plant volatiles: production function and pharmacology. Nat Prod Rep 28:1359–1380PubMedCrossRefPubMedCentralGoogle Scholar
  109. Magazù S, Migliardo F, Benedetto A, La Torre R, Hennet L (2012) Bio-protective effects of homologous disaccharides on biological macromolecules. Eur Biophys J 41(4):361–367PubMedCrossRefPubMedCentralGoogle Scholar
  110. Mahfoozi S, Limin AE, Fowler DB (2001) Developmental regulation of low-temperature tolerance in winter wheat. Ann Bot 87:751–757CrossRefGoogle Scholar
  111. Mahfoozi S, Limin AE, Ahakpaz F, Fowler DB (2006) Phenological development and expression of freezing resistance in spring and winter wheat under field conditions in north-west Iran. Field Crop Res 97(2):182–187CrossRefGoogle Scholar
  112. Mäntylä E, Lång V, Palva ET (1995) Role of abscisic acid in drought-induced freezing tolerance cold acclimation and accumulation of LTI78 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148PubMedPubMedCentralCrossRefGoogle Scholar
  113. Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). J Plant Growth Regul 34(1):135–148CrossRefGoogle Scholar
  114. 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(6):982–993PubMedPubMedCentralCrossRefGoogle Scholar
  115. Mazzucotelli E, Tartari A, Cattivelli L, Forlani G (2006) Metabolism of γ-aminobutyric acid during cold acclimation and freezing and its relationship to frost tolerance in barley and wheat. J Exp Bot 57(14):3755–3766PubMedCrossRefPubMedCentralGoogle Scholar
  116. Megha S, Basu U, Kav NN (2014) Metabolic engineering of cold tolerance in plants. Biocatal Agric Biotechnol 3(1):88–95CrossRefGoogle Scholar
  117. Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175PubMedPubMedCentralCrossRefGoogle Scholar
  118. Morin X, Ameglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, Miglietta F, Chuine I (2007) Variation in cold hardiness and carbohydrate concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27:817–825PubMedCrossRefPubMedCentralGoogle Scholar
  119. Morsy MR, Jouve L, Hausman JF, Hoffmann L, Stewart JM (2007) Alteration of oxidative and carbohydrate metabolism under abiotic stress in two rice (Oryza sativa L.) genotypes contrasting in chilling tolerance. J Plant Physiol 164(2):157–167PubMedCrossRefPubMedCentralGoogle Scholar
  120. Nägele T, Stutz S, Hörmiller II, Heyer AG (2012) Identification of a metabolic bottleneck for cold acclimation in Arabidopsis thaliana. Plant J 72(1):102–114PubMedCrossRefPubMedCentralGoogle Scholar
  121. Nagler M, Nukarinen E, Weckwerth W, Nägele T (2015) Integrative molecular profiling indicates a central role of transitory starch breakdown in establishing a stable C/N homeostasis during cold acclimation in two natural accessions of Arabidopsis thaliana. BMC Plant Biol 15(1):284PubMedPubMedCentralCrossRefGoogle Scholar
  122. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway. Int J Mol Sci 16(12):30117–30132PubMedPubMedCentralCrossRefGoogle Scholar
  123. Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annu Rev Plant Biol 51(1):111–140CrossRefGoogle Scholar
  124. Niinemets U, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9(4):180–186PubMedCrossRefPubMedCentralGoogle Scholar
  125. Niinemets U (2010) Mild versus severe stress and BVOCs: thresholds priming and consequences. Trends Plant Sci 15:145–153PubMedCrossRefPubMedCentralGoogle Scholar
  126. Ninagawa T, Eguchi A, Kawamura Y, Konishi T, Narumi A (2016) A study on ice crystal formation behavior at intracellular freezing of plant cells using a high-speed camera. Cryobiology 73(1):20–29PubMedCrossRefPubMedCentralGoogle Scholar
  127. Ogasawara N, Hiramasu T, Ishiyama K, Fushimi H, Suzuki H, Takagi H (2001) Effects of gibberellic acid and temperature on growth and root carbohydrates of Delphinium seedlings. J Plant Growth Regul 33(3):181–187CrossRefGoogle Scholar
  128. Okumoto S, Funck D, Trovato M, Forlani G (2016) Amino acids of the glutamate family: functions beyond primary metabolism. Front Plant Sci 7:318PubMedPubMedCentralCrossRefGoogle Scholar
  129. Park EJ, Jeknić Z, Sakamoto A, DeNoma J, Yuwansiri R, Murata N, Chen TH (2004) Genetic engineering of glycinebetaine synthesis in tomato protects seeds plants and flowers from chilling damage. Plant J 40(4):474–487PubMedCrossRefPubMedCentralGoogle Scholar
  130. Partelli FL, Vieira HD, Rodrigues APD, Pais I, Campostrini E, Chaves MMCC, Ramalho JC (2010) Cold induced changes on sugar contents and respiratory enzyme activities in coffee genotypes. Ciência Rural 40(4):781–786CrossRefGoogle Scholar
  131. Pasandi M, Janmohammadi M (2015) Effects of cold-hardening and plant developments on freezing tolerance of winter plants in a cold climate. Curr Opin Agric 4(1):10–18Google Scholar
  132. Peshev D, Vergauwen R, Moglia A, Hideg É, Van den Ende W (2013) Towards understanding vacuolar antioxidant mechanisms: a role for fructans. J Exp Bot 64(4):1025–1038PubMedPubMedCentralCrossRefGoogle Scholar
  133. Pirzadah TB, Malik B, Rehman RU, Hakeem KR, Qureshi MI (2014) Signaling in response to cold stress. In: Plant signaling: understanding the molecular crosstalk. Springer, New Delhi, pp 193–226Google Scholar
  134. Pramanik MH, 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 58:751–762CrossRefGoogle Scholar
  135. Prášil IT, Kadlecová-Faltusová Z, Faltus M (2001) Water and ABA content in fully expanded leaves of cold-hardened barleys. Icel Agric Sci 14:49–53Google Scholar
  136. Puhakainen T (2004) Physiological and molecular analyses of cold acclimation of plants. University of Helsinki, FinlandGoogle Scholar
  137. Purdy SJ, Bussell JD, Nunn CP, Smith SM (2013) Leaves of the Arabidopsis maltose exporter1 mutant exhibit a metabolic profile with features of cold acclimation in the warm. PLoS One 8:e79412PubMedPubMedCentralCrossRefGoogle Scholar
  138. Rácz I, Páldi E, Szalai G, Janda T, Pál M, Lásztity D (2008) S-methylmethionine reduces cell membrane damage in higher plants exposed to low-temperature stress. J Plant Physiol 165(14):1483–1490PubMedCrossRefPubMedCentralGoogle Scholar
  139. Rai VK, Sharma UD (1991) Amino acids can modulate ABA induced stomatal closure stomatal resistance and K+ fluxes in Vicia faba leaves. Beitr Biol Pflanz 66:393–405Google Scholar
  140. Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45(4):481–487CrossRefGoogle Scholar
  141. Rao RSP, Andersen JR, Dionisio G, Boelt B (2011) Fructan accumulation and transcription of candidate genes during cold acclimation in three varieties of Poa pratensis. J Plant Physiol 168(4):344–351PubMedCrossRefPubMedCentralGoogle Scholar
  142. Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59(15):4205–4217PubMedPubMedCentralCrossRefGoogle Scholar
  143. Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars: metabolism sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4(5):388–393PubMedPubMedCentralCrossRefGoogle Scholar
  144. Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67PubMedCrossRefGoogle Scholar
  145. Ryu SB, Costa A, Xin Z, Li PH (1995) Induction of cold hardiness by salt stress involves synthesis of cold- and abscisic acid-responsive proteins in potato (Solanum Commersonii Dun). Plant Cell Physiol 36:1245–1251Google Scholar
  146. Sah SK, Kaur G, Wani SH (2016) Metabolic engineering of compatible solute trehalose for abiotic stress tolerance in plants. In: Osmolytes and plants acclimation to changing environment: emerging Omics technologies. Springer, New Delhi, pp 83–96CrossRefGoogle Scholar
  147. Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25(2):163–171PubMedCrossRefPubMedCentralGoogle Scholar
  148. Samanta A, Das G, Das SK (2011) Roles of flavonoids in plants. Int J Pharm Sci Technol 6:12–35Google Scholar
  149. Savitch LV, Gray GR, Huner NP (1997) Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201(1):18–26CrossRefGoogle Scholar
  150. Schneider T, Keller F (2009) Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant Cell Physiol 50(12):2174–2182PubMedCrossRefPubMedCentralGoogle Scholar
  151. Schulz E, Tohge T, Zuther E, Fernie AR, Hincha DK (2016) Flavonoids are determinants of freezing tolerance and cold acclimation in Arabidopsis thaliana. Sci Rep 6:34027PubMedPubMedCentralCrossRefGoogle Scholar
  152. Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436PubMedCrossRefPubMedCentralGoogle Scholar
  153. Sharma N, Cram D, Huebert T, Zhou N, Parkin IA (2007) Exploiting the wild crucifer Thlaspi arvense to identify conserved and novel genes expressed during a plant’s response to cold stress. Plant Mol Biol 63(2):171–184PubMedCrossRefPubMedCentralGoogle Scholar
  154. Shen B, Hohmann S, Jensen RG, Bohnert HJ (1999) Roles of sugar alcohols in osmotic stress adaptation. Replacement of glycerol by mannitol and sorbitol in yeast. Plant Physiol 121(1):45–52PubMedPubMedCentralCrossRefGoogle Scholar
  155. Shi J, Fu XZ, Peng T, Huang XS, Fan QJ, Liu JH (2010) Spermine pretreatment confers dehydration tolerance of citrus in vitro plants via modulation of antioxidative capacity and stomatal response. Tree Physiol 30(7):914–922PubMedCrossRefPubMedCentralGoogle Scholar
  156. Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98(3):565–571PubMedPubMedCentralCrossRefGoogle Scholar
  157. Singh BD (2014) Plant breeding: principles and methods. Kalyani Publishers, New DelhiGoogle Scholar
  158. Slewinski TL (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. J Exp Bot 63(13):4647–4670PubMedCrossRefGoogle Scholar
  159. Smallwood M, Bowles DJ (2002) Plants in a cold climate. Philos Trans R Soc Lond Ser B Biol Sci 357:831–847CrossRefGoogle Scholar
  160. Solanke AU, Sharma AK (2008) Signal transduction during cold stress in plants. Physiol Mol Biol Plants 14(1–2):69–79PubMedPubMedCentralCrossRefGoogle Scholar
  161. Stefanowska M, Kuraś M, Kacperska A (2002) Low temperature-induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves. Ann Bot 90(5):637–645PubMedPubMedCentralCrossRefGoogle Scholar
  162. Strimbeck GR, Schaberg PG, Fossdal CG, Schröder WP, Kjellsen TD (2015) Extreme low temperature tolerance in woody plants. Front Plant Sci 6:884PubMedPubMedCentralCrossRefGoogle Scholar
  163. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  164. Takahashi T, Kakehi JI (2010) Polyamines: ubiquitous polycations with unique roles in growth and stress responses. Ann Bot 105(1):1–6PubMedCrossRefPubMedCentralGoogle Scholar
  165. Tapernoux-Lüthi EM, Böhm A, Keller F (2004) Cloning functional expression and characterization of the raffinose oligosaccharide chain elongation enzyme galactan: galactan galactosyltransferase from common bugle leaves. Plant Physiol 134(4):1377–1387PubMedPubMedCentralCrossRefGoogle Scholar
  166. Tarkowski ŁP, Van den Ende W (2015) Cold tolerance triggered by soluble sugars: a multifaceted countermeasure. Front Plant Sci 6:203PubMedPubMedCentralCrossRefGoogle Scholar
  167. Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235(6):1091–1105CrossRefGoogle Scholar
  168. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599PubMedCrossRefPubMedCentralGoogle Scholar
  169. Turhan E, Ergin S (2012) Soluble sugars and sucrose-metabolizing enzymes related to cold acclimation of sweet cherry cultivars grafted on different rootstocks. Sci World J 2012 Article 7 pagesGoogle Scholar
  170. Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2(2):79–85PubMedPubMedCentralCrossRefGoogle Scholar
  171. Valle RVB (2002) Mechanisms of frost adaptation and freeze damage in grapevine buds. PhD dissertation Hohenheim UniversityGoogle Scholar
  172. Van Velthuizen H (2007) Mapping biophysical factors that influence agricultural production and rural vulnerability (No. 11). Food & Agriculture OrganizationGoogle Scholar
  173. Verbruggen N, Hermans C (2008) Proline accumulation in plants: a review. Amino Acids 35(4):753–759PubMedCrossRefGoogle Scholar
  174. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291PubMedCrossRefPubMedCentralGoogle Scholar
  175. Wani SH, Brajendra Singh N, Haribhushan A, Iqbal Mir J (2013) Compatible solute engineering in plants for abiotic stress tolerance-role of glycine betaine. Curr Genomics 14(3):157–165PubMedPubMedCentralCrossRefGoogle Scholar
  176. Wani SH, Sah SK, Hossain MA, Kumar V, Balachandran SM (2016) Transgenic approaches for abiotic stress tolerance in crop plants. In: Advances in plant breeding strategies: agronomic abiotic and biotic stress traits. Springer, Cham, pp 345–396CrossRefGoogle Scholar
  177. Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23(9):893–902CrossRefGoogle Scholar
  178. Xing W, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46(1):21–28PubMedCrossRefPubMedCentralGoogle Scholar
  179. Yadav SK (2010) Cold stress tolerance mechanisms in plants. A review. Agron Sustain Dev 30(3):515–527CrossRefGoogle Scholar
  180. Yue C, Cao HL, Wang L, Zhou YH, Huang YT, Hao XY, Wang YC, Wang B, Yang YJ, Wang XC (2015) Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88(6):591–608CrossRefGoogle Scholar
  181. Yuki M, Grukhin V, Lee CS, Haworth IS (1996) Spermine binding to GC-rich DNA: experimental and theoretical studies. Arch Biochem Biophys 325(1):39–46PubMedCrossRefPubMedCentralGoogle Scholar
  182. Zhang J, Wu X, Niu R, Liu Y, Liu N, Xu W, Wang Y (2012) Cold-resistance evaluation in 25 wild grape species. Vitis 51(4):153–160Google Scholar
  183. Zhang W, Jiang B, Li W, Song H, Yu Y, Chen J (2009) Polyamines enhance chilling tolerance of cucumber (Cucumis sativus L.) through modulating antioxidative system. Sci Hortic 122(2):200–208CrossRefGoogle Scholar
  184. Zhao H, Yang H (2008) Exogenous polyamines alleviate the lipid peroxidation induced by cadmium chloride stress in Malus hupehensis Rehd. Sci Hortic 116:442–447CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Valentina Longo
    • 1
  • Mohsen Janmohammadi
    • 2
  • Lello Zolla
    • 3
  • Sara Rinalducci
    • 4
    Email author
  1. 1.National Research Council, Institute for Microelectronics and MicrosystemsLecceItaly
  2. 2.Department of Plant Production and GeneticsAgriculture College, University of MaraghehMaraghehIran
  3. 3.Department of Science and Technology for Agriculture, Forestry, Nature and Energy (DAFNE)University of TusciaViterboItaly
  4. 4.Department of Ecological and Biological Sciences (DEB)University of TusciaViterboItaly

Personalised recommendations