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Low-temperature stress: is phytohormones application a remedy?

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Abstract

Among the various abiotic stresses, low temperature is one of the major environmental constraints that limit the plant development and crop productivity. Plants are able to adapt to low-temperature stress through the changes in membrane composition and activation of reactive oxygen scavenging systems. The genetic pathway induced due to temperature downshift is based on C-repeat-binding factors (CBF) which activate promoters through the C-repeat (CRT) cis-element. Calcium entry is a major signalling event occurring immediately after a downshift in temperature. The increase in the level of cytosolic calcium activates many enzymes, such as phospholipases and calcium dependent-protein kinases. MAP-kinase module has been shown to be involved in the cold response. Ultimately, the activation of these signalling pathways leads to changes in the transcriptome. Several phytohormones, such as abscisic acid, brassinosteroids, auxin, salicylic acid, gibberellic acid, cytokinins and jasmonic acid, have been shown to play key roles in regulating the plant development under low-temperature stress. These phytohormones modulate important events involved in tolerance to low-temperature stress in plants. Better understanding of these events and genes controlling these could open new strategies for improving tolerance mediated by phytohormones.

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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

    Article  CAS  Google Scholar 

  • Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193

    Article  CAS  Google Scholar 

  • Aghdam MS, Mohammadkhani N (2014) Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food Bioproc Technol 7:909–914

    Article  CAS  Google Scholar 

  • Aghdam MS, Asghari M, Farmani B, Mohayeji M, Moradbeygi H (2012) Impact of postharvest brassinosteroids treatment on PAL activity in tomato fruit in response to chilling stress. Sci Hortic 144:116–120

    Article  CAS  Google Scholar 

  • Ahammed GJ, Yuan HL, Ogweno JO, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ (2012) Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato. Chemosphere 86:546–555

    Article  CAS  Google Scholar 

  • Ahmed CB, Rouina BB, Sensoy S, Boukhriss M, Abdullah FB (2010) Exogenous proline effects on photosynthetic performance and antioxidant defense system of young olive tree. J Agric Food Chem 58:4216–4222

    Article  CAS  Google Scholar 

  • Allen RD (1995) Dissection of oxidative stress tolerance using transgenic plants. Plant Physiol 107:1049–1054

    Article  CAS  Google Scholar 

  • Al-Taisan WA (2010) Comparative effects of drought and salt stress on germination and seedling growth of Pennisetum divisum (Gmel.) Henr. Am J Appl Sci 7:640–646

    Article  Google Scholar 

  • Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P (2000) Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev 146(1):2085–2096

    Google Scholar 

  • Arroyo A, Bossi F, Finkelstein RR, Leon P (2003) Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in Arabidopsis. Plant Physiol 1336(1):231–242

    Article  CAS  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216

    Article  CAS  Google Scholar 

  • Baena-Gonzalez E, Gray JC, Tyystjarvi E, Aro EM, Maenpaa P (2001) Abnormal regulation of photosynthetic electron transport in a chloroplast ycf9 inactivation mutant. J Biol Chem 276:20795–20802

    Article  CAS  Google Scholar 

  • Bajguz A (2000) Effect of brassinosteroids on nucleic acid and protein content in cultured cell of Chlorella vulgaris. Plant Physiol Biochem 38:209–215

  • Bajguz A (2009) Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J Plant Physiol 166:882–886

    Article  CAS  Google Scholar 

  • Banu NA, Hoque A, Watanabe-Sugimoto M, Islam MM, Uraji M, Matsuoka K, Nakamura Y, Murata Y (2010) Proline and glycine betaine ameliorated NaCl stress via scavenging of hydrogen peroxide and methylglyoxal but not superoxide or nitric oxide in tobacco cultured cells. Biosci Biotechnol Biochem 74:2043–2049

    Article  CAS  Google Scholar 

  • Bauerfeind MA, Winkelmann T, Franken P, Druege U (2015) Transcriptome, carbohydrate, and phytohormone analysis of Petunia hybrida reveals a complex disturbance of plant functional integrity under mild chilling stress. Front Plant Sci https://doi.org/10.3389/fpls.2015.00583

  • Belin C, Megies C, Hauserova E, Lopez-Molina L (2009) Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell 21:2253–2268

    Article  CAS  Google Scholar 

  • Biao WN (2006) Alleviating effects of exogenous salicylic acid (SA) on chilling stress in radish. J Southwest Agric Univ 28:782–785

    Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91:179–194

    Article  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. ASPP, Rockville, MD, pp 1158–1249

    Google Scholar 

  • Calegario FF, Cosso RG, Fagian MM, Almeida FV, Jardim WF, Jezˇek P, Arruda P, Vercesi AE (2003) Stimulation of potato tuber respiration by cold stress is associated with an increased capacity of both plant uncoupling mitochondrial protein (PUMP) and alternative oxidase. J Bioenerg Biomembr 35:211–220

    Article  CAS  Google Scholar 

  • Cao S, Zheng Y, Wang K, Jin P, Rui H (2009) Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem 115:1458−1463

  • Carvallo MA, Pino MT, Jeknic Z, Zou C, Doherty CJ, Shiu SH, Chen TH, Thomashow MF (2011) A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 62:3807–3819

    Article  CAS  Google Scholar 

  • Chandler JW (2009) Auxin as compere in plant hormone crosstalk. Planta 231:1–12

    Article  CAS  Google Scholar 

  • Chen S, Zimei L, Cui J, Jiangang D, Xia X, Liu D, Yu J (2011) Alleviation of chilling-induced oxidative damage by salicylic acid pretreatment and related gene expression in eggplant seedlings. Plant Growth Regul 65:101–108

    Article  CAS  Google Scholar 

  • Cheng WH, Endo A, Zhou L, Penney J, Chen HC, Arroyo A, Leon P, Nambara E, Asami T, Seo M, Koshiba T, Sheen J (2002) A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions. Plant Cell 146(1):2723–2743

    Article  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  Google Scholar 

  • Cui C, Zhou QY (2013) Antioxidant enzyme and morphological characteristics of roots of three Nicotiana tabacum L. genotype seedlings under chilling stress. Afr J Agr Res 8:64–69

    Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  Google Scholar 

  • Dat J, Vandenabeele S, Vranova E, Montagu MV, Inze D, Breusegem FV (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  Google Scholar 

  • Davière JM, de Lucas M, Prat S (2008) Transcriptional factor interaction: a central step in DELLA function. Curr Opin Genet Dev 18:295–303

    Article  CAS  Google Scholar 

  • Davies PJ (1995) The plant hormones: their nature, occurrence, and functions. In: Davies PJ (ed) Plant hormones: physiology, biochemistry and molecular biology, 2nd edn. Kluwer Academic Publisher’s, Dordrecht, pp 1–12

    Chapter  Google Scholar 

  • Del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335

    Article  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Curr Biol 21:R365–R373

    Article  CAS  Google Scholar 

  • DeRidder BP, Crafts-Brandner SJ (2008) Chilling stress response of post-emergent cotton seedlings. Physiol Plant 134:430–439

    Article  CAS  Google Scholar 

  • Derkx MPM, Vermeer E, Karssen CM (1994) Gibberellins in seeds of Arabidopsis thaliana: biological activities, identification and effects of light and chilling on endogenous levels. Plant Growth Regul 15:223–234

    Article  CAS  Google Scholar 

  • Ding CK, Wang CY, Gross KC, Smith DL (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901

    Article  CAS  Google Scholar 

  • Equiza MA, Miravé JP, Tognetti JA (2001) Morphological, anatomical and physiological responses related to differential shoot vs. root growth inhibition at low temperature in spring and winter wheat. Ann Bot 87:67–76

    Article  Google Scholar 

  • Fariduddin Q, Yusuf M, Chalkoo S, Hayat S, Ahmad A (2011) 28-Homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica 49:55–64

    Article  CAS  Google Scholar 

  • Farooq M, Aziz T, Basra SMA, Cheema MA, Rehman H (2008) Chilling tolerance in hybrid maize induced by seed priming with salicylic acid. J Agron Crop Sci 194:161–168

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Basra SMA, Din I (2009) Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 195:262–269

    Article  CAS  Google Scholar 

  • Feng L, Zhao YH, Wang F, Zhang L (2003) Effects study on MeJA treatment for cold storage of peach. Food Sci 9:135–139

    Article  Google Scholar 

  • Finkelstein RR, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Ann Rev Plant Biol 59:387–415

    Article  CAS  Google Scholar 

  • Fiorani F, Umbach LA, Siedow NJ (2005) The AOX of plant mitochondria is involved in the acclimation of shoot growth at low temperature. A study of Arabidopsis AOX1a transgenic plants. Plant Physiol 139:1795–1805

    Article  CAS  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant morphogenesis. Curr Opin Plant Biol 8:77–85

    Article  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  CAS  Google Scholar 

  • Foolad MR, Lin GY (2001) Genetic analysis of cold tolerance during vegetative growth in tomato, Lycopersicon esculentum Mill. Euphytica 122:105–111

    Article  Google Scholar 

  • Galiba G, Tuberosa R, Kocsy G, Sutka J (1993) Involvement of chromosome 5A and chromosome 5D in cold-induced abscisic acid accumulation in and frost tolerance of wheat calli. Plant Breed 110:237–242

    Article  CAS  Google Scholar 

  • Gamalei YV, Van Bel AJE, Pakhomova MV, Sjutkina AV (1994) Effects of temperature on the conformation of the endoplasmic reticulum and on starch accumulation in leaves with the symplasmic minor-vein configuration. Planta 194:443–453

    Article  CAS  Google Scholar 

  • Gao H, Zhang ZK, Lv XG, Cheng N, Peng BZ, Cao W (2016) Effect of 24-epibrassinolide on chilling injury of peach fruit in relation to phenolic and proline metabolisms. Post Biol Technol 111:390–397

    Article  CAS  Google Scholar 

  • Garstka M, Venema JH, Runiak I, Gieczewska K, Rosiak M, Koziol-Lipinska J, Kierdaszuk B, Vredenberg WJ, Mostowska A (2007) Contrasting effect of dark-chilling on chloroplast structure and arrangement of chlorophyll-protein complexes in pea and tomato: plants with a different susceptibility to non-freezing temperature. Planta 226:1165–1181

    Article  CAS  Google Scholar 

  • Genard H, Le Saos J, Hillard J, Tremolieres A, Boucaud J (1991) Effect of salinity on lipid composition, glycine betaine content and photosynthetic activity in chloroplasts of Suaeda maritime. Plant Physiol Biochem 29:421–427

    CAS  Google Scholar 

  • Gharib FA, Hegazi AZ (2010) Salicylic acid ameliorates germination, seedling growth, phytohormone and enzymes activity in bean (Phaseolus vulgaris L.) under cold stress. J Am Sci 6:675–683

    Google Scholar 

  • Ghorbani B, Pakkish Z (2014) Brassinosteroid enhances cold stress tolerance of Washington navel orange (Citrus sinensis L.) fruit by regulating antioxidant enzymes during storage. Agric Conspec Sci 79:109–114

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  CAS  Google Scholar 

  • 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 124:1854–1865

    Article  CAS  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardestrom P, Schroder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. Plant J 47:720–734

    Article  CAS  Google Scholar 

  • Guda CD, Scordo E, Allera C, Farina E (2000) Effects of low temperatures and gibberellic acid on flowering of Limonium gmelinii. Acta Hortic 541:323–326

    Article  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, NY

    Google Scholar 

  • Hardtke CS, Dorcey E, Osmont KS, Sibout R (2007) Phytohormone collaboration: zooming in on auxin–brassinosteroid interactions. Trends Cell Biol 17:485–492

    Article  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • He YL, Liu YL, Cao WX, Huai MF, Xu BG, Huang BR (2005) Effects of salicylic acid on heat tolerance associated with antioxidant metabolism in Kentucky Bluegrass. Crop Sci 45(3):988–995

    Article  CAS  Google Scholar 

  • Hedden P, Kamiya Y (1997) Gibberellin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460

    Article  CAS  Google Scholar 

  • Hsu SY, Hsu YT, Kao CH (2003) The effect of polyethylene glycol on proline accumulation in rice leaves. Biol Plant 46:73–78

    Article  CAS  Google Scholar 

  • Hu WH, Zhou YD, Du YS, Xia XJ, Yu JQ (2006) Differential response of photosynthesis in greenhouse and field ecotypes of tomato to long-term chilling under low light. J Plant Physiol 163:1238–1246

    Article  CAS  Google Scholar 

  • Hu WH, Wu Y, Zeng JZ, He L, Zeng QM (2010) Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pre-treatment in cucumber during chilling and subsequent recovery. Photosynthetica 48:537–544

    Article  CAS  Google Scholar 

  • Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of CBF expression–c-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25:2907–2924

    Article  CAS  Google Scholar 

  • Hudak J, Salaj J (1999) Effect of low temperatures on the structure of plant cells. In: Pessarakli M (ed) Handbook of plant and crop stress, 2nd edn. Marcel Dekker Press, New York, pp 441–464

    Google Scholar 

  • Iordachescu M, Imai R (2008) Trehalose biosynthesis in response to abiotic stresses. J Int Plant Biol 50:1223–1229

    Article  CAS  Google Scholar 

  • Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Tari I, Paldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208(2):175–180

    Article  CAS  Google Scholar 

  • Janeczko A, Gullner G, Skoczowski A, Dubert F, Barna B (2007) Effects of brassinosteroid infiltration prior to cold treatment on ion leakage and pigment contents in rape leaves. Biol Plant 51:355–358

    Article  CAS  Google Scholar 

  • Jarmuszkiewicz W, Sluse-Goffart CM, Vercesi AE, Sluse FE (2001) AOX and uncoupling protein: thermogenesis versus cell energy balance. Biosci Rep 21:213–222

    Article  CAS  Google Scholar 

  • Jiang YP, Huang LF, Cheng F, Zhou YH, Xia XJ, Mao WH (2013) Brassinosteroids accelerate recovery of photosynthetic apparatus from cold stress by balancing the electron partitioning, carboxylation and redox homeostasis in cucumber. Physiol Plant 14:133–145

    Article  CAS  Google Scholar 

  • Johnsen K, Maier C, Sanchez F, Anderson P, Butnor J, Waring R, Linder S (2007) Physiological girdling of pine trees via phloem chilling: proof of concept. Plant Cell Environ 30:128–134

    Article  CAS  Google Scholar 

  • Kang GZ, Wang CH, Sun GC, Wang ZX (2003) Salicylic acid changes activities of H2O2-metabolizing enzymes and increases the chilling-tolerance of banana seedlings. Environ Exp Bot 50:9–15

    Article  CAS  Google Scholar 

  • Kang GZ, Zhu GH, Peng XX, Sun GC, Wang ZX (2004) Isolations of salicylic acid-induced genes in chilling-stressed banana seedling leaves using mRNA differential display. J Plant Physiol Mol Biol 30(2):225–228

    CAS  Google Scholar 

  • Kavi Kishore PB, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    Google Scholar 

  • Keith CN, McKersie BD (1986) The effect of abscisic acid on the freezing tolerance of callus cultures of Lotus corniculatus L. Plant Physiol 80:766–770

    Article  CAS  Google Scholar 

  • Khan W, Prithiviraj B, Smith DL (2003) Photosynthetic responses of corn and soybean to foliar application of salicylates. J Plant Physiol 160:485–492

    Article  CAS  Google Scholar 

  • Khan TA, Fariduddin Q, Yusuf M, Ahmad A (2014) Low-temperature triggered varied antioxidant responses in tomato. Int J Veg Sci 21:329–343

    Article  Google Scholar 

  • Khan TA, Fariduddin Q, Yusuf M (2015) Lycopersicon esculentum under low temperature stress: an approach toward enhanced antioxidants and yield. Environ Sci Pollut Res 22:14178–14188

    Article  CAS  Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis Book 12:e0168

    Article  Google Scholar 

  • 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 17:89–95

    Article  CAS  Google Scholar 

  • Ko R, Smith LT, Smith GM (1994) Glycine betaine confers enhanced osmotolerance and cryotolerance in Listeria monocytogenes. J Bacteriol 176:426–431

    Article  CAS  Google Scholar 

  • Korkmaz A, Dufault RJ (2001) Developmental consequences of cold temperature stress at transplanting on seedling and field growth and yield. I. Watermelon. J Am Soc Hortic Sci 126(4):404–409

    Google Scholar 

  • Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NP (1999) Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the Chlorina f2 mutant. Plant Physiol 120:193–204

    Article  CAS  Google Scholar 

  • Kumar M, Sirhindi G, Bhardwaj R, Kumar S, Jain G (2010) Effect of exogenous H2O2 on antioxidant enzymes of Brassica juncea L. seedlings in relation to 24-epibrassinolide under chilling stress. Ind J Biochem Biophys 47:378–382

    CAS  Google Scholar 

  • Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84:692–695

    Article  CAS  Google Scholar 

  • Leon P, Sheen J (2003) Sugar and hormone connections. Trends Plant Sci 86(1):110–116

    Article  CAS  Google Scholar 

  • Levitt J (1980) Responses of plants to environmental stresses. In: Chilling, Freezing, and High Temperature Stresses, vol 1, 2nd edn. Academic Press, New York, p 497

    Google Scholar 

  • Li R, Zhang J, Li J, Zhou G, Wang Q, Bian W, Erb M, Lou Y (2015) Prioritizing plant defence over growth through WRKY regulation facilitates infestation by non-target herbivores. Elife 4:e04805

  • Liu YJ, Zhao ZG, Si J, Di CX, Han J, An LZ (2009) Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. Plant Growth Regul 59:207–214

    Article  CAS  Google Scholar 

  • Liu C, Zhao L, Yu G (2011) The dominant glutamic acid metabolic flux to produce gamma-amino butyric acid over proline in Nicotiana tabacum leaves under water stress relates to its significant role in antioxidant activity. J Integ Plant Biol 53:608–618

    Article  CAS  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. BBA- Rev Biomembr 1666:142–157

    Article  CAS  Google Scholar 

  • Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138

    Article  CAS  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Odadoi K (2004) Dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellins biosynthesis because of over expression of a putative AP2 transcription factor. Plant J 37:720–729

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Maqsood A, Shahbaz M, Akram NA (2006) Influence of exogenously applied glycine betaine on growth and gas exchange characteristics of maize (Zea mays L.) Pak J Agric Sci 43:36–41

    Google Scholar 

  • Marangoni AG, Palma T, Stanley DW (1996) Membrane effects in postharvest physiology. Postharvest Biol Technol 7:193–217

    Article  Google Scholar 

  • Mauger JP (2012) Role of the nuclear envelope in calcium signalling. Biol Cell 104:70–83

    Article  CAS  Google Scholar 

  • McCarthy-Suarez I, Gómez M, Del Río LA, Palma JM (2011) Role of peroxisomes in the oxidative injury induced by the auxin herbicide 2, 4-D in leaves of pea plants. Biol Plant 55:485–492

    Article  CAS  Google Scholar 

  • Medina J, Catala R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11

    Article  CAS  Google Scholar 

  • Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527–543

    Article  CAS  Google Scholar 

  • Millenaar FF, Lambers H (2003) The AOX: in vivo regulation and function. Plant Biol 5:2–15

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591

    Article  Google Scholar 

  • Moore AL, Albury MS, Crichton PG, Affourtit C (2002) Function of the AOX: is it still a scavenger? Trends Plant Sci 7:478–481

    Article  CAS  Google Scholar 

  • Muday GK, Rahman A, Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends Plant Sci 17(4):181–195

    Article  CAS  Google Scholar 

  • Murphy C, Wilson JM (1981) Ultrastructural features of chilling injury in Episcia reptans. Plant Cell Environ 4:261–265

    Google Scholar 

  • Mutlu S, Karadagoglu Ö, Atici Ö, Nalbantoglu B (2013) Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. Biol Plant 57:507–513

    Article  CAS  Google Scholar 

  • Nadella V, Shipp MJ, Muday GK, Wyatt SE (2006) Evidence for altered polar and lateral auxin transport in the gravity persistent signal (gps) mutants of Arabidopsis. Plant Cell Environ 29:682–690

    Article  CAS  Google Scholar 

  • Nägele T, Kandel BA, Frana S, Meissner M, Heyer AG (2011) A systems biology approach for the analysis of carbohydrate dynamics during acclimation to low temperature in Arabidopsis thaliana. FEBS J 278:506–518

    Article  CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:1460–1471

    Article  CAS  Google Scholar 

  • 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 149:28–38

  • Nemhauser JL, Hong FX, Chory J (2006) Different plant hormones regulate similar processes through largely non overlapping transcriptional responses. Cell 126:467–475

    Article  CAS  Google Scholar 

  • Neuhofer W, Beck FX (2006) Survival in hostile environments: strategies of renal medullary cells. Physiology 21:171–180

    Article  CAS  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and GSH: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • 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. Plant Growth Regul 33:181–187

    Article  CAS  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  CAS  Google Scholar 

  • Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono M, Kwbo A, Kanna M, Ioki M, Kamada H, Saji H (2005) Salicylic acid accumulation under O3 exposure is regulated by ethylene in tobacco plants. Plant Cell Physiol 46(7):1062–1072

    Article  CAS  Google Scholar 

  • Okuma E, Murakami Y, Shimoishi Y, Tada M, Murata Y (2004) Effects of exogenous application of proline and betaine on the growth of tobacco cultured cells under saline conditions. Soil Sci Plant Nutr 50:1301–1305

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ozturk L, Demir Y (2002) In vivo and in vitro protective role of proline. Plant Growth Regul 38:259–264

    Article  CAS  Google Scholar 

  • Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100

    Article  CAS  Google Scholar 

  • Pauwels L, Morreel K, De Witte E, Lammertyn F, Van Montagu M, Boerjan W (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci U S A 105:1380–1385

    Article  CAS  Google Scholar 

  • Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424

    Article  CAS  Google Scholar 

  • Plaxton WC (2004) Plant response to stress: biochemical adaptation to phosphate deficiency. Encycl. Plant Crop Sci. Marcel Dekker, New York. pp 976–980.

  • Prasad T, Anderson M, Steward C (1994) Acclimation, hydrogen peroxide, and abscisic acid protect mitochondria against irreversible chilling injury in maize seedlings. Plant Physiol 105:619–627

    Article  CAS  Google Scholar 

  • Purvis AC, Shewfelt RL (1993) Does the alternative pathway ameliorate chilling injury in sensitive plant tissues? Physiol Plant 88:712–718

    Article  CAS  Google Scholar 

  • Qi YH, Yamauchi Y, Ling JQ, Kawano N, Li DB, Tanaka K (2004) Cloning of a putative monogalactosyldiacylglycerol synthase gene from rice (Oryza sativa L.) plants and its expression in response to submergence and other stresses. Planta 219:450–458

    CAS  Google Scholar 

  • Qi F, Li J, Duan L, Li Z (2005) Inductions of coronatine and MeJA to low-temperature resistance of wheat seedlings. Acta Botan Boreali-Occiden Sin 26:1776–1780

    Google Scholar 

  • Rahman A (2013) Auxin: a regulator of cold stress response. Physiol Plant 147:28–35

    Article  CAS  Google Scholar 

  • Rakhmankulova ZF, Fedyaev VV, Rakhmatulina SR, Ivanov CP, Gilvanova IR, Usmanov IY (2010) The effect of wheat seed presowing treatment with salicylic acid on its endogenous content, activities of respiratory pathways, and plant antioxidant status. Russ J Plant Physiol 57:778–783

    Article  CAS  Google Scholar 

  • Reinbothe C, Springer A, Samol I, Reinbothe S (2009) Plant oxylipins: role of jasmonic acid during programmed cell death, defence and leaf senescence. FEBS J 276:4666–4681

    Article  CAS  Google Scholar 

  • Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher-plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384

    Article  CAS  Google Scholar 

  • Robinson SP, Jones GP (1986) Accumulation of glycine betaine in chloroplasts provides osmotic adjustment during salt stress. Aust J Plant Physiol 13:659–668

    Article  CAS  Google Scholar 

  • Rodríguez VM, Soengas P, Alonso-Villaverde V, Sotelo T, Cartea ME, Velasco P (2015) Effect of temperature stress on the early vegetative development of Brassica oleracea L. BMC Plant Biol. https://doi.org/10.1186/s12870-015-0535-0

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

    Article  Google Scholar 

  • Rymen B, Fiorani F, Kartal F, Vandepoele K, Inze D, Beemster GT (2007) Cold nights impair leaf growth and cell cycle progression in maize through transcriptional changes of cell cycle genes. Plant Physiol 143:1429–1438

    Article  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

    Article  CAS  Google Scholar 

  • Sakata T, Oda S, Tsunaga Y, Shomura H, Kawagishi-Kobayashi M, Aya K, Saeki K, Endo T, Nagano K, Kojima M, Sakakibara H, Watanabe M, Matsuoka M, Higashitani A (2014) Reduction of gibberellin by low temperature disrupts pollen development in rice. Plant Physiol 164:2011–2019

    Article  CAS  Google Scholar 

  • Salinas J (2002) Molecular mechanisms of signal transduction in cold acclimation. In: Plant Signal Transduction. Scheel D, Wasternack C. (eds.) Oxford University Press. pp 116–139.

  • Saltveit ME (2002) The rate of ion leakage from chilling-sensitive tissue does not immediately increase upon exposure to chilling temperatures. Post Biol Technol 26:295–304

    Article  CAS  Google Scholar 

  • Sandve SR, Kosmala A, Rudi H, Fjellheim S, Rapacz M, Yamada T, Rognli OA (2011) Molecular mechanisms underlying frost tolerance in perennial grasses adapted to cold climates. Plant Sci 180:69–77

    Article  CAS  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30–43

    Article  CAS  Google Scholar 

  • Sangwan V, Foulds I, Singh J, Dhindsa RS (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

    Article  CAS  Google Scholar 

  • Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–2317

    Article  CAS  Google Scholar 

  • Senaratna T, Touchell D, Bunn T, Dixon K (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Reg 30(2):157–161

    Article  CAS  Google Scholar 

  • Setia RC, Dhanda A, Setia N (2006) Chilling tolerance and related antioxidant enzyme activities induced by salicylic acid in leaves of Brassica juncea (L.) Czern and Coss. Environ Ecol 24:886–889

    Google Scholar 

  • Shah F, Huang J, Cui K, Nie L, Shah T, Chen C, Wang K (2011) Impact of high-temperature stress on rice plant and its traits related to tolerance. Agric Sci 149(05):545–556

  • Shao HB, Liang ZS, Shao MA (2006) Osmotic regulation of 10 wheat (Triticum aestivum L.) genotypes at soil water deficits. Colloid Surf B Biointerfaces 47:132–139

    Article  CAS  Google Scholar 

  • Shao HB, Chu LY, Shao MA, Zhao CX (2008) Advances in functional regulation mechanisms of plant aquaporins: their diversity, gene expression, localization, structure and roles in plant soil-water relations (Review). Mol Membr Biol 25:1–12

    Article  CAS  Google Scholar 

  • Sharifi P (2010) Evaluation on sixty-eight rice germplasms in cold tolerance at germination stage. Rice Sci 17:77–81

    Article  Google Scholar 

  • Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21:3823–3838

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular response to drought and cold stress. Curr Opin Plant Biol 7:161–167

    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

    Article  CAS  Google Scholar 

  • Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560–3573

    Article  CAS  Google Scholar 

  • Sieger SM, Kristensen BK, Robson CA, Amirsadeghi S, Eng EW, Abdel-Mesih A, Møller IM, Vanlerberghe GC (2005) The role of AOX in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56:1499–1515

    Article  CAS  Google Scholar 

  • Siminovitch D (1981) Common and disparate elements in the processes of adaptation of herbaceous and woody plants to freezing: a perspective. Cryobiology 18:166–185

    Article  CAS  Google Scholar 

  • Sińska I, Lewak S, Gaskin P, MacMillan J (1973) Reinvestigation of apple-seed gibberellins. Planta 114:359–364

    Article  Google Scholar 

  • Skinner JS, Von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger E, Thomashow M, Chen THH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551

    Article  CAS  Google Scholar 

  • Skulachev VP (1999) Anion carriers in fatty acid mediated physiological uncoupling. J Bioenerg Biomembr 31:431–445

    Article  CAS  Google Scholar 

  • Somersalo S, Kyei-Boahen S, Pehu E (1996) Exogenous glycine betaine application as a possibility to increase low temperature tolerance of crop plants. Nordisk Jordbruksforskning 78:10

    Google Scholar 

  • Stanca AM, Crosatti C, Grossi M, Lacerenza NG, Rizza F, Cattivelli L (1996) Molecular adaptation of barley to cold and drought conditions. Euphytica 92:215–219

    Article  Google Scholar 

  • Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the cor15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Nat Acad Sci USA 95:14570–14575

    Article  CAS  Google Scholar 

  • Stoll M, Loveys B, Dry P (2000) Hormonal changes induced by partial root zone drying of irrigated grapevine. J Exp Bot 51:1627–1634

    Article  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

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  Google Scholar 

  • Tasgin E, Atici O, Nalbantoglu B, Popova LP (2006) Effects of salicylic acid and cold treatments on protein levels and on the activities of antioxidant enzymes in the apoplast of winter wheat leaves. Phytochemistry 67:710–715

    Article  CAS  Google Scholar 

  • Taylor J, Bhalla M, Robertson J, Piening L (1990) Cytokinins and abscisic acid in hardening winter wheat. Can J Bot 68:1597–1601

    Article  CAS  Google Scholar 

  • Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environ Exp Bot 67:429–443

    Article  CAS  Google Scholar 

  • Theocharis A, Bordiec S, Fernandez O, Paquis S, Dhondt-Cordelier S, Baillieul F, Clement C, Ait BE (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low non-freezing temperatures. Mol Plant Microbe Interact 25:241–249

    Article  CAS  Google Scholar 

  • Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8

    Article  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93

    Article  CAS  Google Scholar 

  • Townley HE, Knight MR (2002) Calmodulin as a potential negative regulator of Arabidopsis COR gene expression. Plant Physiol 128:1169–1172

    Article  CAS  Google Scholar 

  • Tripathi SK, Tuteja N (2007) Integrated signaling in flower senescence. Plant Signal Behav 2:437–445

    Article  Google Scholar 

  • Tuteja N, Mahajan S (2007) Further characterization of calcineurin B-like protein and its interacting partner CBL-interacting protein kinase from Pisum sativum. Plant Signal Behav 2:358–361

    Article  Google Scholar 

  • Usadel B, Bläsing OE, GibonY PF, Höhne M, Günter M (2008) Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ 31:518–547

    Article  CAS  Google Scholar 

  • Valluru R, Link J, Claupein W (2012) Consequences of early chilling stress in two Triticum species: plastic responses and adaptive significance. Plant Biol 14:641–651

    Article  CAS  Google Scholar 

  • Van Heerden PDR, Kruger GHJ, Loveland JE, Parry MAJ, Foyer CH (2003) Dark chilling imposes metabolic restrictions on photosynthesis in soybean. Plant Cell Environ 26:323–337

    Article  Google Scholar 

  • Vanlerberghe GC, Vanlerberghe AE, Mclntosh L (1997) Molecular genetic evidence of the ability of AOX to support respiratory carbon metabolism. Plant Physiol 11:657–661

    Article  Google Scholar 

  • Venema JH, Posthumus F, De Vries M, Van Hasselt PR (1999a) Differential response of domestic and wild Lycopersicon species to chilling under low light: growth, carbohydrate content, photosynthesis and the xanthophyll cycle. Physiol Plant 105:81–88

    Article  CAS  Google Scholar 

  • Venema JH, Posthumus F, van Hasselt PR (1999b) Impact of suboptimal temperature on growth, photosynthesis, leaf pigments and carbohydrates of domestic and high-altitude wild Lycopersicon species. J Plant Physiol 155:711–718

    Article  CAS  Google Scholar 

  • Verbruggen N, Hermans C (2008) Proline accumulation implants: a review. Amino Acids 35:753–759

    Article  CAS  Google Scholar 

  • Vercesi AE (2001) The discovery of an uncoupling mitochondrial protein in plants. Biosci Rep 21:195–200

    Article  CAS  Google Scholar 

  • Veselova SV, Farhutdinov RG, Veselov SY, Kudoyarova GR, Veselov DS, Hartung W (2005) The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.) J Plant Physiol 162:21–26

    Article  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

    Article  CAS  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad M (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Article  Google Scholar 

  • Wan B, Lin Y, Mon T (2007) Expression of rice Ca2+ -dependent protein kinases (CDPKS) genes under different environmental stresses. FEBS Lett 581:1179–1189

  • Wang LJ, Li SH (2006) Salicylic acid-induced heat or cold tolerance in relation to Ca2+ homeostasis and antioxidant systems in young grape plants. Plant Sci 170:685–694

    Article  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  Google Scholar 

  • Wang Y, Yang ZM, Zhang QF, Li JL (2009) Enhanced chilling tolerance in Zoysia matrella by pre-treatment with salicylic acid, calcium chloride, hydrogen peroxide or 6-benzylaminopurine. Biol Plant 53:179–182

    Article  CAS  Google Scholar 

  • Wang Q, Ding T, Gao L, Pang J, Yang N (2012) Effect of brassinolide on chilling injury of green bell pepper in storage. Sci Hortic 144:195–200

    Article  CAS  Google Scholar 

  • Wanner L, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–399

    Article  CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  CAS  Google Scholar 

  • Watanabe T, Kume T (2009) A general adaptation strategy for climate change impacts on paddy cultivation: special reference to the Japanese context. Paddy Water Environ 7:313–320

    Article  Google Scholar 

  • WeiBing X, Rajashekar CB (2001) Glycine betaine involvement in freezing tolerance and water stress in Arabidopsis thaliana. Environ Exp Bot 46:21–28

    Article  Google Scholar 

  • Wilkinson S, Davies WJ (2009) Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. Plant Cell Environ 32:949–959

    Article  CAS  Google Scholar 

  • Willcox JK, Ash SL, Catignani GL (2004) Antioxidants and prevention of chronic disease. Crit Rev Food Sci Nutr 44:275–295

    Article  CAS  Google Scholar 

  • Williams PM, Bradbeer JW, Gaskin P, MacMillan J (1974) Studies in seed dormancy. VIII. The identification and determination of gibberellins A1 and A9 in seed of Corylus avellana L. Planta 117:101–108

    Article  CAS  Google Scholar 

  • Wilson TP, Canny MJ, McCully ME, Lefkovitch LP (1990) Breakdown of cytoplasmic vacuoles: a model of endoplasmic membrane rearrangement. Protoplasma 155:144–152

    Article  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  CAS  Google Scholar 

  • Wisniewski M, Londow SE, Ashworth EN (1997) Observations of ice nucleation and propagation in plants using infrared video thermography. Plant Physiol 113:327–334

    Article  CAS  Google Scholar 

  • Wolters H, Jurgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317

    Article  CAS  Google Scholar 

  • Wyatt SE, Rashotte AM, Shipp MJ, Robertson D, Muday GK (2002) Mutations in the gravity persistence signal loci in Arabidopsis disrupt the perception and/or signal transduction of gravitropic stimuli. Plant Physiol 130:1426–1435

    Article  CAS  Google Scholar 

  • Xi Z, Wang Z, Fang Y, Hu Z, Hu Y, Deng M (2013) Effects of 24-epibrassinolide on antioxidation defense and osmoregulation systems of young grapevines (V. vinifera L.) under chilling stress. Plant Growth Regul 71:57–65

    Article  CAS  Google Scholar 

  • Xia JC, Zhao H, Liu WZ, Li LG, He YK (2009) Role of cytokinin and salicylic acid in plant growth at low temperatures. Plant Growth Regul 57:211–221

    Article  CAS  Google Scholar 

  • Xin Z, Browse J (2001) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Article  Google Scholar 

  • Xin Z, Li PH (1993) Relationship between proline and abscisic acid in the induction of chilling tolerance in maize suspension-cultured cells. Plant Physiol 103:607–613

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  CAS  Google Scholar 

  • Xu Q, Truong TT, Barrero JM, Jacobsen JV, Hocart CH, Gubler F (2016) A role for jasmonates in the release of dormancy by cold stratification in wheat. J Exp Bot 67:3497–3508

    Article  CAS  Google Scholar 

  • Xue-Xuan X, Hong-Bo S, Yuan-Yuan M, Gang X, Jun-Na S, Dong-Gang G (2010) Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abiotic-stressed conditions. Crit Rev Biotechnol 30:222–230

    Article  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

    Article  CAS  Google Scholar 

  • Yamaryo Y, Kanai D, Awai K, Shimojima M, Masuda T, Shimada H, Takamiya K, Ohta H (2003) Light and cytokinin play a co-operative role in MGDG synthesis in greening cucumber cotyledons. Plant Cell Physiol 44:844–855

    Article  CAS  Google Scholar 

  • Yang X, Lu C (2005) Photosynthesis is improved by exogenous glycine betaine in salt-stressed maize plants. Physiol Plant 124:343–352

    Article  CAS  Google Scholar 

  • Yang WJ, Rich PJ, Axtell JD, Wood KV, Bonham CC, Ejeta G, Mickelbart MV, Rhodes D (2003) Genotypic variation for glycine betaine in sorghum. Crop Sci 43:162–169

    Article  CAS  Google Scholar 

  • Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136:1039–1048

    Article  CAS  Google Scholar 

  • Yu XC, Li MJ, Gao GF, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579

    Article  CAS  Google Scholar 

  • Zhang C, Tian S (2009) Crucial contribution of membrane lipids unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0 °С. Food Chem 115:411–415

    Google Scholar 

  • Zhang X, Fowler SG, Cheng H, Lou Y, Rhee SY, Stockinger EJ, Thomashow MF (2004) Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. Plant J 39:905–919

    Article  CAS  Google Scholar 

  • Zhang S, Yang C, Peng J, Sun S, Wang X (2009) GASA5, a regulator of flowering time and stem growth in Arabidopsis thaliana. Plant Mol Biol 69:745–759

    Article  CAS  Google Scholar 

  • Zhang Q, Zhang JZ, Chow WS, Sun LL, Chen JW, Chen YJ, Peng CL (2011a) The influence of low temperature on photosynthesis and antioxidant enzymes in sensitive banana and tolerant plantain (Musa sp.) Photosynthetica 49:201–208

    Article  CAS  Google Scholar 

  • Zhang A, Zhang J, Zhang J, Ye N, Zhang H, Tan M, Jiang M (2011b) Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiol 52(1):181–192

    Article  CAS  Google Scholar 

  • Zhang XD, Wang RP, Zhang FJ, Tao FQ, Li WQ (2013) Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana. Biol Plant 57:149–153

    Article  CAS  Google Scholar 

  • Zhao M, Wang J, Shan W, Fan J, Kuang J, Wu K, Li X, Chen W, He F, Chen J, Lu W (2013) Induction of jasmonate signalling regulators MaMYC2 and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36:30–51

    Article  CAS  Google Scholar 

  • Zolfagharinasab R, Hadian J (2007) Influence of methyl jasmonate on inducing chilling tolerance in pomegranate fruits (Malas Save). Pak J Biol Sci 10:612–616

    Article  CAS  Google Scholar 

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The authors gratefully acknowledge financial support provided by the Council of Science and Technology, Uttar Pradesh [Project No. CST/D-615], India, to carry out this study.

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  1. Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, 202002, India

    Tanveer Alam Khan, Qazi Fariduddin & Mohammad Yusuf

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  1. Tanveer Alam Khan
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  2. Qazi Fariduddin
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Correspondence to Qazi Fariduddin.

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Khan, T.A., Fariduddin, Q. & Yusuf, M. Low-temperature stress: is phytohormones application a remedy?. Environ Sci Pollut Res 24, 21574–21590 (2017). https://doi.org/10.1007/s11356-017-9948-7

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