Skip to main content
SpringerLink
Log in

Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Sugar plays an essential role in plant cold acclimation (CA), but the interaction between CA and sugar remains unclear in tea plants. In this study, during the whole winter season, we investigated the variations of sugar contents and the expression of a large number of sugar-related genes in tea leaves. Results indicated that cold tolerance of tea plant was improved with the development of CA during early winter season. At this stage, starch was dramatically degraded, whereas the content of total sugars and several specific sugars including sucrose, glucose and fructose were constantly elevated. Beyond the CA stage, the content of starch was maintained at a low level during winter hardiness (WH) period and then was elevated during de-acclimation (DC) period. Conversely, the content of sugar reached a peak at WH stage followed by a decrease during DC stage. Moreover, gene expression results showed that, during CA period, sugar metabolism-related genes exhibited different expression pattern, in which beta-amylase gene (CsBAM), invertase gene (CsINV5) and raffinose synthase gene (CsRS2) engaged in starch, sucrose and raffinose metabolism respectively were solidly up-regulated; the expressions of sugar transporters were stimulated in general except the down-regulations of CsSWEET2, 3, 16, CsERD6.7 and CsINT2; interestingly, the sugar-signaling related CsHXK3 and CsHXK2 had opposite expression patterns at the early stage of CA. These provided comprehensive insight into the effects of CA on carbohydrates indicating that sugar accumulation contributes to tea plant cold tolerance during winter season, and a simply model of sugar regulation in response to cold stimuli is proposed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Afoufa-Bastien D, Medici A, Jeauffre J, Coutos-Thevenot P, Lemoine R, Atanassova R, Laloi M (2010) The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol 10:245

    Article  PubMed Central  PubMed  Google Scholar 

  • Andersen MN, Asch F, Wu Y, Jensen CR, Naested H, Mogensen VO, Koch KE (2002) Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol 130:591–604

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bae H, Herman E, Bailey B, Bae HJ, Sicher R (2005) Exogenous trehalose alters Arabidopsis transcripts involved in cell wall modification, abiotic stress, nitrogen metabolism, and plant defense. Physiol Plant 125:114–126

    Article  CAS  Google Scholar 

  • Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482

    Article  PubMed Central  PubMed  Google Scholar 

  • Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942

    Article  CAS  PubMed  Google Scholar 

  • Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–2037

    Article  CAS  PubMed  Google Scholar 

  • Browse J, Xin Z (2001) Temperature sensing and cold acclimation. Curr Opin Plant Biol 4:241–246

    Article  CAS  PubMed  Google Scholar 

  • Cao YY, Yang MT, Li X, ZhouZQ WangXJ, Bai JG (2014) Exogenous sucrose increases chilling tolerance in cucumber seedlings by modulating antioxidant enzyme activity and regulating proline and soluble sugar contents. Sci Hortic 179:67–77

    Article  CAS  Google Scholar 

  • Chardon F, Bedu M, Calenge F, Klemens PA, Spinner L, Clement G, Chietera G, Leran S, Ferrand M, Lacombe B, Loudet O, Dinant S, Bellini C, Neuhaus HE, Daniel-Vedele F, Krapp A (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol CB 23:697–702

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155

    Article  CAS  PubMed  Google Scholar 

  • Chen LQ, Cheung LS, Feng L, Tanner W, Frommer WB (2015) Transport of Sugars. Annu Rev Biochem 84:865–894

    Article  PubMed  Google Scholar 

  • Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Davik J, Koehler G, From B, Torp T, Rohloff J, Eidem P, Wilson RC, Sonsteby A, Randall SK, Alsheikh M (2013) Dehydrin, alcohol dehydrogenase, and central metabolite levels are associated with cold tolerance in diploid strawberry (Fragaria spp.). Planta 237:265–277

    Article  CAS  PubMed  Google Scholar 

  • Egert A, Keller F, Peters S (2013) Abiotic stress-induced accumulation of raffinose in Arabidopsis leaves is mediated by a single raffinose synthase (RS5, At5g40390). BMC Plant Biol 13:218

    Article  PubMed Central  PubMed  Google Scholar 

  • Espevig T, DaCosta M, Hoffman L, Aamlid TS, Tronsmo AM, Clarke BB, Huang B (2011) Freezing tolerance and carbohydrate changes of two Agrostis species during cold acclimation. Crop Sci 51:1188–1197

    Article  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci 99:15898–15903

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gong X, Liu M, Zhang L, Ruan Y, Ding R, Ji Y, Zhang N, Zhang S, Farmer J, Wang C (2015) Arabidopsis AtSUC2 and AtSUC4, encoding sucrose transporters, are required for abiotic stress tolerance in an ABA-dependent pathway. Physiol Plant 153:119–136

  • Granot D, David-Schwartz R, Kelly G (2013) Hexose kinases and their role in sugar-sensing and plant development. Front Plant Sci 4:44

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hao XY, Horvath D, Chao W, Yang YY, Wang XC, Xiao B (2014) Identification and evaluation of reliable reference genes for quantitative real-time PCR analysis in tea plant (Camellia sinensis (L.) O. Kuntze). Int J Mol Sci 15:22155–22172

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang YW, Nie YX, Wan YY, Chen SY, Sun Y, Wang XJ, Bai JG (2013) Exogenous glucose regulates activities of antioxidant enzyme, soluble acid invertase and neutral invertase and alleviates dehydration stress of cucumber seedlings. Sci Hortic 162:20–30

    Article  CAS  Google Scholar 

  • Ibraheem O, Botha CEJ, Bradley G (2010) In silico analysis of cis-acting regulatory elements in 5′ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput Biol Chem 34:268–283

    Article  CAS  PubMed  Google Scholar 

  • Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5–19

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, Kim YS, Seo HS, Choi YD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jossier M, Bouly J-P, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59:316–328

    Article  CAS  PubMed  Google Scholar 

  • Kaplan F, Guy CL (2004) beta-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135:1674–1684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44:730–743

    Article  CAS  PubMed  Google Scholar 

  • Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kaplan F, Sung DY, Guy CL (2006) Roles of β-amylase and starch breakdown during temperatures stress. Physiol Plant 126:120–128

    Article  CAS  Google Scholar 

  • Kasuga J, Arakawa K, Fujikawa S (2007) High accumulation of soluble sugars in deep supercooling Japanese white birch xylem parenchyma cells. New Phytol 174:569–579

    Article  CAS  PubMed  Google Scholar 

  • Keunen E, Peshev D, Vangronsveld J, Van den Ende W, Cuypers A (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255

    Article  CAS  PubMed  Google Scholar 

  • Klemens PA, Patzke K, Deitmer JW, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus E (2013a) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth and stress tolerance in Arabidopsis thaliana. Plant Physiol 163:1338–1352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klemens PA, Patzke K, Trentmann O, Poschet G, Buttner M, Schulz A, Marten I, Hedrich R, Neuhaus HE (2013b) Over expression of a proton-coupled vacuolar glucose exporter impairs freezing tolerance and seed germination. New Phytol 202:188–202

    Article  PubMed  Google Scholar 

  • Klotke J, Kopka J, Gatzke N, Heyer AG (2004) Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation–evidence for a role of raffinose in cold acclimation. Plant Cell Environ 27:1395–1404

    Article  CAS  Google Scholar 

  • Knaupp M, Mishra K, Nedbal L, Heyer AG (2011) Evidence for a role of raffinose in stabilizing photosystem II during freeze–thaw cycles. Planta 234:477–486

    Article  CAS  PubMed  Google Scholar 

  • Laby RJ, Kim D, Gibson SI (2001) The ram1 mutant of Arabidopsis exhibits severely decreased beta-amylase activity. Plant Physiol 127:1798–1807

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee JH, Yu DJ, Kim SJ, Choi D, Lee HJ (2012) Intraspecies differences in cold hardiness, carbohydrate content and beta-amylase gene expression of Vaccinium corymbosum during cold acclimation and deacclimation. Tree Physiol 32:1533–1540

    Article  CAS  PubMed  Google Scholar 

  • Lemoine R, La Camera S, Atanassova R, Dedaldechamp F, Allario T, Pourtau N, Bonnemain JL, Laloi M, Coutos-Thevenot P, Maurousset L, Faucher M, Girousse C, Lemonnier P, Parrilla J, Durand M (2013) Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272

    Article  PubMed Central  PubMed  Google Scholar 

  • Li XW, Feng ZG, Yang HM, Zhu XP, Liu J, Yuan HY (2010) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt-and dehydration-tolerance in tobacco. Biochem Biophys Res Commun 394:354–359

    Article  CAS  PubMed  Google Scholar 

  • 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 4:361–374

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396

    Article  CAS  PubMed  Google Scholar 

  • Lloyd J, Blennow A, Burhenne K, Kossmann J (2004) Repression of a novel isoform of disproportionating enzyme (stDPE2) in potato leads to inhibition of starch degradation in leaves but not tubers stored at low temperature. Plant Physiol 134:1347–1354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lundmark M, Cavaco AM, Trevanion S, Hurry V (2006) Carbon partitioning and export in transgenic Arabidopsis thaliana with altered capacity for sucrose synthesis grown at low temperature: a role for metabolite transporters. Plant Cell Environ 29:1703–1714

    Article  CAS  PubMed  Google Scholar 

  • Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336

    Article  CAS  PubMed  Google Scholar 

  • Nagao M, Matsui K, Uemura M (2008) Klebsormidium flaccidum, a charophycean green alga, exhibits cold acclimation that is closely associated with compatible solute accumulation and ultrastructural changes. Plant Cell Environ 31:872–885

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Zhu XF, Fan QJ, Sun PP, Liu JH (2012) Identification and characterization of low temperature stress responsive genes in Poncirus trifoliata by suppression subtractive hybridization. Gene 492:220–228

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Zhu X, Duan N, Liu JH (2014) PtrBAM1, a beta-amylase-coding gene of Poncirus trifoliata, is a CBF regulon member with function in cold tolerance by modulating soluble sugar levels. Plant Cell Environ 202:188–197

    Google Scholar 

  • 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:e79412

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ramon M, Rolland F, Sheen J (2008) Sugar sensing and signaling. The Arabidopsis Book:e0117

  • Rekarte-Cowie I, Ebshish OS, Mohamed KS, Pearce RS (2008) Sucrose helps regulate cold acclimation of Arabidopsis thaliana. J Exp Bot 59:4205–4217

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Rosa M, Prado C, Podazza G, Interdonato R, Gonzalez JA, Hilal M, Prado FE (2009) Soluble sugars–metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4:388–393

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ruan YL (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol 65:33–67

    Article  CAS  PubMed  Google Scholar 

  • Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yeld potential, and response to drought and heat. Mol Plant 3:942–955

    Article  CAS  PubMed  Google Scholar 

  • Sambe MA, He X, Tu Q, Guo Z (2015) A cold-induced myo-inositol transporter-like gene (MfINT-like) confers tolerance to multiple abiotic stresses in transgenic tobacco plants. Physiol Plant 153:355–364

    Article  CAS  PubMed  Google Scholar 

  • Schulze WX, Schneider T, Starck S, Martinoia E, Trentmann O (2012) Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J 69:529–541

    Article  CAS  PubMed  Google Scholar 

  • Sicher R (2011) Carbon partitioning and the impact of starch deficiency on the initial response of Arabidopsis to chilling temperatures. Plant Sci 181:167–176

    Article  CAS  PubMed  Google Scholar 

  • Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279

    Article  CAS  PubMed  Google Scholar 

  • Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293

    Article  PubMed Central  PubMed  Google Scholar 

  • Thomashow MF (1999) PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  Google Scholar 

  • 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 2012:979682

    Article  Google Scholar 

  • Unda F, Canam T, Preston L, Mansfield SD (2012) Isolation and characterization of galactinol synthases from hybrid poplar. J Exp Bot 63:2059–2069

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F (2011) Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62:545–555

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valluru R, Van den Ende W (2011) Myo-inositol and beyond—emerging networks under stress. Plant Sci 181:387–400

    Article  CAS  PubMed  Google Scholar 

  • Valluru R, Lammens W, Claupein W, Van den Ende W (2008) Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Sci 13:409–414

    Article  CAS  PubMed  Google Scholar 

  • Van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4:247

    Article  PubMed  Google Scholar 

  • Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60:9–18

    Article  PubMed  Google Scholar 

  • Wang H, Ma F, Cheng L (2010) Metabolism of organic acids, nitrogen and amino acids in chlorotic leaves of ‘Honeycrisp’ apple (Malus domestica Borkh) with excessive accumulation of carbohydrates. Planta 232:511–522

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Jiang CJ, Li YY, Wei CL, Deng WW (2012) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis. Plant Cell Rep 31:27–34

    Article  PubMed  Google Scholar 

  • Wang XC, Zhao QY, Ma CL, Zhang ZH, Cao HL, Kong YM, Yue C, Hao XY, Chen L, Ma JQ, Jin JQ, Li X, Yang YJ (2013) Global transcriptome profiles of Camellia sinensis during cold acclimation. BMC Genom 14:415

    Article  Google Scholar 

  • Williams LE, Lemoine R, Sauer N (2000) Sugar transporters in higher plants—a diversity of roles and complex regulation. Trends Plant Sci 5:283–290

    Article  CAS  PubMed  Google Scholar 

  • Wood IP, Elliston A, Ryden P, Bancroft I, Roberts IN, Waldron KW (2012) Rapid quantification of reducing sugars in biomass hydrolysates: Improving the speed and precision of the dinitrosalicylic acid assay. Biomass Bioenergy 44:117–121

    Article  CAS  Google Scholar 

  • Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476–3490

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu LH, Zhou MQ, Shen C, Liang J, Lin J (2012) Transgenic tobacco plants over expressing cold regulated protein CbCOR15b from Capsella bursa-pastoris exhibit enhanced cold tolerance. J Plant Physiol 169:1408–1416

    Article  CAS  PubMed  Google Scholar 

  • Xiang L, Le Roy K, Bolouri-Moghaddam M-R, Vanhaecke M, Lammens W, Rolland F, Van den Ende W (2011) Exploring the neutral invertase–oxidative stress defence connection in Arabidopsis thaliana. J Exp Bot 62:3849–3862

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461

    Article  CAS  PubMed  Google Scholar 

  • Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902

    Article  Google Scholar 

  • Xu PL, Guo YK, Bai JG, Shang L, Wang XJ (2008) Effects of long-term chilling on ultrastructure and antioxidant activity in leaves of two cucumber cultivars under low light. Physiol Plant 132:467–478

    Article  CAS  PubMed  Google Scholar 

  • Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch-related α-glucan/water dikinaseis involved in the cold-induced development of freezing tolerance in Arabidopsis. Plant Physiol 138:837–846

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu X, Peng YH, Zhang MH, Shao YJ, Su WA, Tang ZC (2006) Water relations and an expression analysis of plasma membrane intrinsic proteins in sensitive and tolerant rice during chilling and recovery. Cell Res 16:599–608

    Article  PubMed  Google Scholar 

  • Yue C, Cao H, Wang L, Zhou Y, Hao X, Zeng J, Wang X, Yang Y (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76

    Article  CAS  PubMed  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234

    Article  CAS  PubMed  Google Scholar 

  • Zhang LL, Zhao MG, Tian QY, Zhang WH (2011) Comparative studies on tolerance of Medicago truncatula and Medicago falcata to freezing. Planta 234:445–457

    Article  CAS  PubMed  Google Scholar 

  • Zhuo C, Wang T, Lu S, Zhao Y, Li X, Guo Z (2013) A cold responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol Plant 149:67–78

    Article  CAS  PubMed  Google Scholar 

  • Zuther E, Buchel K, Hundertmark M, Stitt M, Hincha DK, Heyer AG (2004) The role of raffinose in the cold acclimation response of Arabidopsis thaliana. FEBS Lett 576:169–173

    Article  CAS  PubMed  Google Scholar 

  • Zuther E, Schulz E, Childs LH, Hincha DK (2012) Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions. Plant Cell Environ 35:1860–1878

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Prof. Zongmao Chen and Dr. Xinzhong Zhang of the Tea Research Institute of CAAS for their assistance with the GC/MS analysis. This work was supported by the National Natural Science Foundation of China (31170650), the Natural Science Foundation of Zhejiang Province (Z3100473, LY14C160001), the Earmarked Fund for China Agriculture Research System (CARS-23), the Major Project for New Agricultural Varieties Breeding of Zhejiang Province (2012C2905-3) and the Chinese Academy of Agricultural Sciences through an Innovation Project for Agricultural Sciences and Technology.

Author information

Author notes

    Authors and Affiliations

    1. Tea Research Institute of the Chinese Academy of Agricultural Sciences, Hangzhou, 310008, People’s Republic of China

      Chuan Yue, Hong-Li Cao, Lu Wang, Yan-Hua Zhou, Yu-Ting Huang, Xin-Yuan Hao, Yu-Chun Wang, Bo Wang, Ya-Jun Yang & Xin-Chao Wang

    2. Key Laboratory of Tea Biology and Resources Utilization, Ministry of Agriculture, Hangzhou, 310008, People’s Republic of China

      Chuan Yue, Hong-Li Cao, Lu Wang, Yan-Hua Zhou, Yu-Ting Huang, Xin-Yuan Hao, Yu-Chun Wang, Bo Wang, Ya-Jun Yang & Xin-Chao Wang

    3. National Center for Tea Improvement, Hangzhou, 310008, People’s Republic of China

      Lu Wang, Xin-Yuan Hao, Yu-Chun Wang, Bo Wang, Ya-Jun Yang & Xin-Chao Wang

    Authors
    1. Chuan Yue
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Hong-Li Cao
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Lu Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Yan-Hua Zhou
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Yu-Ting Huang
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Xin-Yuan Hao
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Yu-Chun Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. Bo Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. Ya-Jun Yang
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Xin-Chao Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Chuan Yue.

    Additional information

    Chuan Yue, Hong-li Cao and Lu Wang have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 1143 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Yue, C., Cao, HL., Wang, L. et al. Effects of cold acclimation on sugar metabolism and sugar-related gene expression in tea plant during the winter season. Plant Mol Biol 88, 591–608 (2015). https://doi.org/10.1007/s11103-015-0345-7

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11103-015-0345-7

    Keywords

    Search

    Navigation