Skip to main content

Advertisement

SpringerLink
Log in

Proteomics: A tool to decipher cold tolerance

  • Published:
Theoretical and Experimental Plant Physiology Aims and scope Submit manuscript

Abstract

The term ‘proteomics’ refers to a high-throughput technology and methodology to analyze protein profile of any organism. The complete set of proteins (proteome) of a cell is quite complex apart from being dynamic. Furthermore, environmental conditions greatly influence the accumulation of many proteins and thus dissecting the dynamics of proteome in response to any external stimuli is crucial for understanding the plant response to different environmental cues. Cold or freezing stress is a severe abiotic stress that not only reduces crop yield but also restricts the geographical distribution of many plant species on earth. The ability of the plants to adapt to various environmental stresses determines their survival and understanding this ‘ability’ is crucial for developing stress tolerant plants for improving agricultural yield. Proteomics provides an important platform to understand the molecular mechanisms lying behind cold tolerance in different plants. Here we have reviewed the current proteomics studies in plant response to cold stress with specific emphasis to cold stress response in plants at organ and organelle levels.

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

Similar content being viewed by others

Abbreviations

CBF:

Cold binding factor

COR:

Cold responsive

DREB:

Dehydration responsive element binding factor

LEA:

Late embryogenesis abundant protein

AFP:

Anti-freeze protein

HIR:

Hypersensitive induced response

References

  • Afroz A, Ali GM, Mir A, Komatsu S (2011) Application of proteomics to investigate stress-induced proteins for improvement in crop protection. Plant Cell Rep 30:745–763

    Article  CAS  PubMed  Google Scholar 

  • Ahmad P, Jaleel CA, Sharma S (2010) Antioxidant defense system, lipid peroxidation, proline-metabolizing enzymes, and biochemical activities in two Morus alba genotypes subjected to NaCl stress. Russ J Plant Physiol 57:509–517

    Article  CAS  Google Scholar 

  • Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889

    Article  CAS  PubMed  Google Scholar 

  • Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–2513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amara I, Capellades M, Ludevid MD, Pagès M, Goday A (2013) Enhanced water stress tolerance of transgenic maize plants over-expressing LEARab28 gene. J Plant Physiol 170:864–873

    Article  CAS  PubMed  Google Scholar 

  • Amme S, Matros A, Schlesier B, Mock HP (2006) Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology. J Exp Bot 57:1537–1546

    Article  CAS  PubMed  Google Scholar 

  • Amme-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268

    Article  CAS  Google Scholar 

  • Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An F, Li G, Li QX, Li K, Carvalho LJ, Ou W, Chen S (2016) The comparatively proteomic analysis in response to cold stress in cassava plantlets. Plant Mol Biol Rep 34:1095–1110

    Article  CAS  Google Scholar 

  • Anderson JS, Lyon CE, Fox AH, Leung AK, Lam YW, Steen H, Lamond AI (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12:1–11

    Article  Google Scholar 

  • Artlip TS, Callahan AM, Basett CL, Wisniewski ME (1997) Seasonal expression of a dehydrin gene in sibling deciduous and evergreen genotypes of peach (Prunus persica L. Batsch.). Plant Mol Biol 33:61–70

    Article  CAS  PubMed  Google Scholar 

  • Artlip TS, Wisniewski ME, Arora R, Norelli JL (2016) An apple rootstock overexpressing a peach CBF gene alters growth and flowering in the scion but does not impact cold hardiness or dormancy. Hort Res 3:16006

    Article  CAS  Google Scholar 

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404–13409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atıcı Ö, Nalbantoǧlu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Badowiec A, Weidner S (2014) Proteomic changes in the roots of germinating Phaseolus vulgaris seeds in response to chilling stress and post-stress recovery. J Plant Physiol 171:389–398

    Article  CAS  PubMed  Google Scholar 

  • Badowiec A, Swigonska S, Weidner S (2013) Changes in the protein patterns in pea (Pisum sativum L.) roots under the influence of long-and short-term chilling stress and post-stress recovery. Plant Physiol Biochem 71:315–324

    Article  CAS  PubMed  Google Scholar 

  • Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663

    Article  CAS  PubMed  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5#-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    Article  CAS  PubMed  Google Scholar 

  • Bao F, Huang X, Zhu C, Zhang X, Li X, Yang S (2014) Arabidopsis HSP90 protein modulates RPP4-mediated temperature-dependent cell death and defense responses. New Phytol 202:1320–1334

    Article  CAS  PubMed  Google Scholar 

  • Battaglia M, Covarrubias AA (2013) Late embryogenesis abundant (LEA) proteins in legumes. Front Plant Sci 4:190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertrand A, Bipfubusa M, Castonguay Y, Rocher S, Szopinska-Morawska A, Papadopoulos Y, Renaut J (2016) A proteome analysis of freezing tolerance in red clover (Trifolium pratense L.). BMC Plant Biol 16:65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop RE (2000) The bacterial lipocalins. BBA-Protein Struct Molecular Enzymol 1482:73–83

    Article  CAS  Google Scholar 

  • Bosl B, Grimminger V, Walter S (2006) The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J Struct Biol 156:139–148

    Article  CAS  PubMed  Google Scholar 

  • Bravo LA, Gallardo J, Navarrete A, Olave N, Martinez J, Alberdi M et al (2003) Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiol Plant 118:262–269

    Article  CAS  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2008) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucl Acids Res 37((suppl_1)):D233-8

    PubMed  Google Scholar 

  • Chakraborty S, Salekdeh GH, Yang P, Woo SH, Chin CF, Gehring C, Haynes PA, Mirzaei M, Komatsu S (2015) Proteomics of important food crops in the Asia Oceania Region: current status and future perspectives. J Proteome Res 14:2723–2744

    Article  CAS  PubMed  Google Scholar 

  • Chang MY, Chen SL, Lee CF, Chen YM (2001) Cold-acclimation and root temperature protection from chilling injury in chilling-sensitive mungbean seedlings. Bot Bull Acad Sinica. https://doi.org/10.1186/s40529-017-0161-2

    Article  Google Scholar 

  • Chen L, Madura K (2002) Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol 22:4902–4913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen J, Lin T, Xu H, Tian D, Luo Y, Ren C, Yang L, Shi J (2012a) Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis. Plant Omics 5:194

    CAS  Google Scholar 

  • Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012b) The role of WRKY transcription factors in plant abiotic stresses. BBA-Gene Regul Mech 1819:120–128

    CAS  Google Scholar 

  • Chen J, Han G, Shang C, Li J, Zhang H, Liu F, Wang J, Liu H, Zhang Y (2015) Proteomic analyses reveal differences in cold acclimation mechanisms in freezing-tolerant and freezing-sensitive cultivars of alfalfa. Front Plant Sci 6:105

    PubMed  PubMed Central  Google Scholar 

  • Choi DW, Werner-Fraczek J, Fenton RD, Koag MC, Ahmadian S, Malatrasi M, Chin A, Bravo LC, Close TJ (2000) Genetic map locations and expression of the barley dehydrin multigene family. Barley Genet 8:264–265

    Google Scholar 

  • Crecelius F, Streb P, Feierabend J (2003) Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. J Exp Bot 54:1075–1083

    Article  CAS  PubMed  Google Scholar 

  • Crosatti C, Pagani D, Cattivelli L, Stanca AM, Rizza F (2008) Effects of growth stage and hardening conditions on the association between frost resistance and the expression of the cold-induced protein COR14b in barley. Env Exp Bot 62:93–100

    Article  CAS  Google Scholar 

  • Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172

    Article  CAS  PubMed  Google Scholar 

  • Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Die JV, Arora R, Rowland LJ (2016) Global patterns of protein abundance during the development of cold hardiness in blueberry. Environ Exp Bot 124:11–21

    Article  CAS  Google Scholar 

  • Domon JM, Baldwin L, Acket S, Caudeville E, Arnoult S, Zub H, Gillet F, Lejeune-Hénaut I, Brancourt-Hulmel M, Pelloux J, Rayon C (2013) Cell wall compositional modifications of Miscanthus ecotypes in response to cold acclimation. Phytochemistry 85:51–61

    Article  CAS  PubMed  Google Scholar 

  • Dong C, Danyluk J, Wilson KE, Pocock T, Huner NP, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368–1381

    Article  CAS  Google Scholar 

  • Douce R (2012) Mitochondria in higher plants: structure, function, and biogenesis. Elsevier, Amsterdam

    Google Scholar 

  • Duman JG (1994) Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochim Biophys Acta 1206:129–135

    Article  CAS  PubMed  Google Scholar 

  • Dumont E, Bahrman N, Goulas E, Valot B, Sellier H, Hilbert JL, Vuylsteker C, Lejeune-Hénaut I, Delbreil B (2011) A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 180:86–98

    Article  CAS  PubMed  Google Scholar 

  • Dundr M, Misteli T (2002) Nucleolomics: an inventory of the nucleolus. Mol Cell 9:5–7

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espevig T, Xu C, Aamlid TS, DaCosta M, Huang B (2012) Proteomic responses during cold acclimation in association with freezing tolerance of velvet bentgrass. J Am Soc Hortic Sci 137:391–399

    Article  CAS  Google Scholar 

  • Evers D, Legay S, Lamoureux D, Hausman JF, Hoffmann L, Renaut J (2012) Towards a synthetic view of potato cold and salt stress response by transcriptomic and proteomic analyses. Plant Mol Biol 78:503–514

    Article  CAS  PubMed  Google Scholar 

  • Fan Y, Liu B, Wang H, Wang S, Wang J (2002) Cloning of antifreeze protein gene from carrot and its influence on cold tolerance in transgenic tobacco plants. Plant Cell Rep 21:296–301

    Article  CAS  Google Scholar 

  • Fei YB, Cao PX, Gao SQ, Wang B, Wei LB, Zhao J, Chen G, Wang BH (2008) Purification and structure analysis of antifreeze proteins from Ammopiptanthus mongolicus. Prep Biochem Biotechnol 38:179–190

    Article  CAS  Google Scholar 

  • Feng RJ, Zhang LL, Wang JY, Luo JM, Peng M, Qi JF, Zhang YD, Lu LF (2015) Proteomic analysis of cold stress responses in banana leaves. J Am Soc Hortic Sci 140:214–222

    Article  CAS  Google Scholar 

  • Folgado R, Sergeant K, Renaut J, Swennen R, Hausman JF, Panis B (2014) Changes in sugar content and proteome of potato in response to cold and dehydration stress and their implications for cryopreservation. J Proteom 98:99–111

    Article  CAS  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  PubMed Central  Google Scholar 

  • Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low temperature-induced gene expression in barley. Plant Physiol 127:1676–1681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox AH, Lam YW, Leung AK, Lyon CE, Andersen J, Mann M, Lamond AI (2002) Paraspeckles: a novel nuclear domain. Curr Biol 12:13–25

    Article  CAS  PubMed  Google Scholar 

  • Fu L, Ding Z, Han B, Hu W, Li Y, Zhang J (2016) Physiological investigation and transcriptome analysis of polyethylene glycol (PEG)-induced dehydration stress in cassava. Int J Mol Sci 17:283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gammulla CG, Pascovici D, Atwell BJ, Haynes PA (2010) Differential metabolic response of cultured rice (Oryza sativa) cells exposed to high-and low-temperature stress. Proteomics 10:3001–3019

    Article  CAS  PubMed  Google Scholar 

  • Gao F, Zhou Y, Zhu W, Li X, Fan L, Zhang G (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230:1033–1046

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Bañuelos ML, Gardea AA, Winzerling JJ, Vazquez-Moreno L (2009) Characterization of a midwinter-expressed dehydrin (DHN) gene from apple trees (Malus domestica). Plant Mol Biol Rep 27:476

    Article  CAS  Google Scholar 

  • Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371

    Article  CAS  PubMed  Google Scholar 

  • Gharechahi J, Alizadeh H, Naghavi MR, Sharifi G (2014) A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.). Mol Biol Rep 41:3897–3905

    Article  CAS  PubMed  Google Scholar 

  • Ghosh D, Xu J (2014) Abiotic stress responses in plant roots: a proteomics perspective. Front Plant Sci 5:6

    Article  CAS  PubMed  PubMed Central  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  PubMed  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  PubMed  Google Scholar 

  • Gokirmak T, Paul AL, Ferl RJ (2010) Plant phosphopeptide-binding proteins as signaling mediators. Curr Opin Plant Biol 13:527–532

    Article  CAS  PubMed  Google Scholar 

  • Gong SY, Huang GQ, Sun X, Li P, Zhao LL, Zhang DJ, Li XB (2012) GhAGP31, a cotton non-classical arabinogalactan protein, is involved in response to cold stress during early seedling development. Plant Biol 14:447–457

    Article  CAS  PubMed  Google Scholar 

  • Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder 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  PubMed  Google Scholar 

  • Goyal RK, Fatima T, Topuz M, Bernadec A, Sicher R, Handa AK, Mattoo AK (2016) Pathogenesis-related protein 1b1 (PR1b1) is a major tomato fruit protein responsive to chilling temperature and upregulated in high polyamine transgenic genotypes. Front Plant Sci 7:901

    Article  PubMed  PubMed Central  Google Scholar 

  • Graether SP, Boddington KF (2014) Disorder and function: a review of the dehydrin protein family. Front Plant Sci 5:576

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405

    Article  CAS  PubMed  Google Scholar 

  • Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerreiro N, Redmond JW, Rolfe BG, Djordjevic MA (1997) New Rhizobium leguminosarum flavonoid-induced proteins revealed by proteome analysis of differentially displayed proteins. Mol Plant Microbe Interact 10:506–516

    Article  CAS  PubMed  Google Scholar 

  • Guillaumie S, Goffner D, Barbier O, Martinant JP, Pichon M, Barrière Y (2008) Expression of cell wall related genes in basal and ear internodes of silking brown-midrib-3, caffeic acid O-methyltransferase (COMT) down-regulated, and normal maize plants. BMC Plant Biol 8:71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cells. J Exp Bot 58:3829–3840

    Article  CAS  PubMed  Google Scholar 

  • Guo W, Ward RW, Thomashow MF (1992) Characterization of a cold-regulated wheat gene related to Arabidopsis Cor47. Plant Physiol 100:915–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Wang S, Valerius O, Hall H, Zeng Q, Li JF, Chen JG (2011) Involvement of Arabidopsis RACK1 in protein translation and its regulation by abscisic acid. Plant Physiol 155:370–383

    Article  CAS  PubMed  Google Scholar 

  • Guo Q, Lv X, Xu F, Zhang Y, Wang J, Lin H, Wu B (2013) Chlorine dioxide treatment decreases respiration and ethylene synthesis in fresh-cut ‘Hami’melon fruit. Int J Food Sci Technol 48:1775–1782

    Article  CAS  Google Scholar 

  • Gupta R, Deswal R (2012) Low temperature stress modulated secretome analysis and purification of antifreeze protein from Hippophae rhamnoides, a himalayan wonder plant. J Proteome Res 11:2684–2696

    Article  CAS  PubMed  Google Scholar 

  • Gupta R, Deswal R (2014) Antifreeze proteins enable plants to survive in freezing conditions. J Biosci 39:931–944

    Article  CAS  PubMed  Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384

    Article  CAS  PubMed  Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han R, Campbell KP (2007) Dysferlin and muscle membrane repair. Curr Opin Cell Biol 19:409–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Q, Kang G, Guo T (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244

    Article  CAS  PubMed  Google Scholar 

  • Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara M (2010) The multifunctionality of dehydrins: an overview. Plant Signal Behav 5:503–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298

    CAS  PubMed  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662

    Article  CAS  PubMed  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703

    Article  CAS  PubMed  Google Scholar 

  • Harholt J, Suttangkakul A, Scheller HV (2010) Biosynthesis of pectin. Plant Physiol 153:384–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashimoto M, Komatsu S (2007) Proteomic analysis of rice seedlings during cold stress. Proteomics 7:1293–1302

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto M, Toorchi M, Matsushita K, Iwasaki Y, Komatsu S (2009) Proteome analysis of rice root plasma membrane and detection of cold stress responsive proteins. Protein Pept Lett 16:685–697

    Article  CAS  PubMed  Google Scholar 

  • Heidarvand L, Maali-Amiri R (2013) Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. J Plant Physiol 170:459–469

    Article  CAS  PubMed  Google Scholar 

  • 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 57:3601–3618

    Article  CAS  PubMed  Google Scholar 

  • Hinault MP, Goloubinoff P (2007) Molecular crime and cellular punishment. Molecular aspects of the stress response: chaperones, membranes and networks. Springer, New York, pp 47–54

    Chapter  Google Scholar 

  • Hohnjec N, Küster H, Albus U, Frosch SC, Becker JD, Pühler A, Frühling M (2000) The broad bean nodulin VfENOD18 is a member of a novel family of plant proteins with homologies to the bacterial MJ0577 superfamily. Mol Gen Genet 264:241–250

    Article  CAS  PubMed  Google Scholar 

  • Hon WC, Griffith M, Mlynarz A, Kwok YC, Yang DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol 109:879–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43:2393–2416

    Article  CAS  PubMed  Google Scholar 

  • Houde M, Dallaire S, N’Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotechnol J 2:381–387

    Article  CAS  PubMed  Google Scholar 

  • Huang T, Duman JG (2002) Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara. Plant Mol Biol 48:339–350

    Article  CAS  PubMed  Google Scholar 

  • Huang B, Chu CH, Chen SL, Juan HF, Chen YM (2006) A proteomics study of the mung bean epicotyl regulated by brassinosteroids under conditions of chilling stress. Cell Mol Biol Lett 11:264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang S, Millar AH, Taylor NL (2011) The plant mitochondrial proteome composition and stress response: conservation and divergence between monocots and dicots. Plant mitochondria. Springer, New York, NY, pp 207–239

    Chapter  Google Scholar 

  • Huang Y, Jin D, Lu C, Lan X, Qiao P, Li H, Chen Y (2016) Proteomic responses associated with freezing tolerance in the callus of the Tibetan alpine plant Saussurea laniceps during cold acclimation. Plant Cell Tissue Organ Cult 124:81–95

    Article  CAS  Google Scholar 

  • Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47:291–305

    Article  CAS  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imin N, Kerim T, Weinman JJ, Rolfe BG (2006) Low temperature treatment at the young microspore stage induces protein changes in rice anthers. Mol Cell Proteomics 5:274–292

    Article  CAS  PubMed  Google Scholar 

  • Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Nat Acad Sci USA 96:13566–13570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwasaki T, Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1997) The dehydration-inducible Rd17 (Cor47) gene and its promoter region in Arabidopsis thaliana (Accession No. AB004872). Plant Gene Register. Plant Physiol 115:1287–1289

    Article  Google Scholar 

  • Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J Proteome Res 9:6595–6604

    Article  CAS  PubMed  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  CAS  PubMed  Google Scholar 

  • Jain S, Kumar D, Jain M, Chaudhary P, Deswal R, Sarin NB (2012) Ectopic overexpression of a salt stress-induced pathogenesis related class 10 protein (PR10) gene from peanut (Arachis hypogaea L.) affords broad spectrum abiotic stress tolerance in transgenic tobacco. Plant Cell Tiss Organ Cult 109:19–31

    Article  CAS  Google Scholar 

  • Jan N, Qazi H, Ramazan S, John R (2018a) Developing stress tolerant plants through in vitro tissue culture: family brassicaceae. In: Gosal SS, Wani SH (eds) Biotechnologies of crop improvement, volume 1: cellular approaches. Springer Nature, New York

    Google Scholar 

  • Jan N, Wani UM, Andrabi KI, John R (2018b) Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta Physiol Plant 40:73

    Article  CAS  Google Scholar 

  • Janmohammadi M, Mock HP, Matros A (2014) Proteomic analysis of cold acclimation in winter wheat under field conditions. Icel Agric Sci 27:3–15

    Google Scholar 

  • Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: changes at the protein level. Phytochemistry 117:76–89

    Article  CAS  PubMed  Google Scholar 

  • Janska A, Marsík P, Zelenková S, Ovesna J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405

    Article  CAS  PubMed  Google Scholar 

  • Janska A, Aprile A, Zamecník J, Cattivelli L, Ovesna J (2011) Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct Integr Genomics 11:307–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jardim-Messeder D, Caverzan A, Rauber R, de Souza Ferreira E, Margis-Pinheiro M, Galina A (2015) Succinate dehydrogenase (mitochondrial complex II) is a source of reactive oxygen species in plants and regulates development and stress responses. New Phytol 203:776–789

    Article  CAS  Google Scholar 

  • Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802

    Article  CAS  PubMed  Google Scholar 

  • Jarzabeck M, Pukacki PM, Nuc K (2009) Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea spp.). Cryobiology 58:268–274

    Article  CAS  Google Scholar 

  • Ji L, Zhou P, Zhu Y, Liu F, Li R, Qiu Y (2017) Proteomic analysis of rice seedlings under cold stress. Protein J 36:299–307

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Zhang C, Yang H, Yang Y, Huang C, Tian Y, Lu X (2011) Proteomic analysis of cold stress responses in tobacco seedlings. Afr J Biotechnol 10:18991–19004

    Article  CAS  Google Scholar 

  • John R, Anjum NA, Sopory SK, Akram NA, Ashraf M (2016) Some key physiological and molecular processes of cold acclimation. Biol Plant 60:603–618

    Article  CAS  Google Scholar 

  • Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2010) Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism. Progress Lipid Res 49:128–158

    Article  CAS  Google Scholar 

  • Juszczak I, Bartels D (2017) LEA gene expression, RNA stability and pigment accumulation in three closely related Linderniaceae species differing in desiccation tolerance. Plant Sci 255:59–71

    Article  CAS  PubMed  Google Scholar 

  • Kader JC (1997) Lipid-transfer proteins: a puzzling family of plant proteins. Trends Plant Sci 2:66–70

    Article  Google Scholar 

  • Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev 11:579–592

    Article  CAS  Google Scholar 

  • Karami-Moalem S, Maali-Amiri R, Kazemi-Shahandashti SS (2018) Effect of cold stress on oxidative damage and mitochondrial respiratory properties in chickpea. Plant Physiol Biochem 122:31–39

    Article  CAS  PubMed  Google Scholar 

  • Karimzadeh G, Francis D, Davies MS (2000) Low temperature-induced accumulation of protein is sustained both in root meristems and in callus in winter wheat but not in spring wheat. Ann Bot 85:769–777

    Article  CAS  Google Scholar 

  • Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154

    Article  CAS  PubMed  Google Scholar 

  • Kazuoka T, Oeda K (1992) Heat-stable COR (cold-regulated) proteins associated with freezing tolerance in spinach [Spinacia oleracea]. Plant Cell Physiol 33:1107–1114

    CAS  Google Scholar 

  • Kindgren P, Dubreuil C, Strand A (2015) The recovery of plastid function is required for optimal response to low temperatures in Arabidopsis. PLoS ONE 10:e0138010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • King HA, Gerber AP (2014) Translatome profiling: methods for genome-scale analysis of mRNA translation. Brief Funct Genomics 15:22–31

    PubMed  Google Scholar 

  • Kirch HH, Schlingensiepen S, Kotchoni S, Sunkar R, Bartels D (2005) Detailed expression analysis of selected genes of the aldehyde dehydrogenase (ALDH) gene superfamily in Arabidopsis thaliana. Plant Mol Biol 57:315–332

    Article  CAS  PubMed  Google Scholar 

  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1994) Characterization of two cDNAs (ERD10 and ERD14) corresponding to genes that respond rapidly to dehydration stress in Arabidopsis thaliana. Plant Cell Physiol 35:225–231

    CAS  PubMed  Google Scholar 

  • Koehler G, Wilson RC, Goodpaster JV, Sønsteby A, Lai X, Witzmann FA, Alsheikh M (2012) Proteomic study of low-temperature responses in strawberry cultivars (Fragaria × Ananassa) that differ in cold tolerance. Plant Physiol 159:1787–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Komarova TV, Pozdyshev DV, Petrunia IV, Sheshukova EV, Dorokhov YL (2014) Pectin methylesterase-generated methanol may be involved in tobacco leaf growth. Biochemistry (Moscow) 79:102–110

    Article  CAS  Google Scholar 

  • Komatsu S, Yanagawa Y (2013) Cell wall proteomics of crops. Front Plant Sci 4:17

    PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kontogiorgos V, Regand A, Yada RY, Goff HD (2007) Isolation and characterization of ice structuring proteins from cold acclimated winter wheat grass extract for recrystallization inhibition in frozen foods. J Food Biochem 31:139–160

    Article  CAS  Google Scholar 

  • Kosakivska I, Klymchuk D, Negretzky V, Bluma D, Ustinova A (2008) Stress proteins and ultrastructural characteristics of leaf cells of plants with different types of ecological strategies. Gen Appl Plant Physiol 34:405–418

    CAS  Google Scholar 

  • Kosmala A, Bocian A, Rapacz M, Jurczyk B, Zwierzykowski Z (2009) Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance. J Exp Bot 60:3595–3609

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT (2007) The role of dehydrins in plant response to cold. Biol Plant 51:601–617

    Article  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress-contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Urban MO, Prášil IT, Renaut J (2018) Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front Plant Sci 9:122

    Article  PubMed  PubMed Central  Google Scholar 

  • Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78

    Article  CAS  PubMed  Google Scholar 

  • Larance M, Lamond AI (2015) Multidimensional proteomics for cell biology. Nat Rev Mol Cell Biol 16:269

    Article  CAS  PubMed  Google Scholar 

  • 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 57:104–112

    Article  CAS  PubMed  Google Scholar 

  • Le MQ, Pagter M, Hincha DK (2015) Global changes in gene expression, assayed by microarray hybridization and quantitative RT-PCR, during acclimation of three Arabidopsis thaliana accessions to sub-zero temperatures after cold acclimation. Plant Mol Biol 87:1–15

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR (2005) Characterization of an abiotic stress inducible dehydrin gene, OsDhn1, in rice (Oryza sativa L.). Mol Cells 19:212–218

    CAS  PubMed  Google Scholar 

  • Lee SC, Kim SH, An SH, Yi SY, Hwang BK (2006) Identification and functional expression of the pepper pathogen-induced gene, CAPIP2, involved in disease resistance and drought and salt stress tolerance. Plant Mol Biol 62:151–164

    Article  CAS  PubMed  Google Scholar 

  • Lee DG, Ahsan N, Lee SH, Lee JJ, Bahk JD, Kang KY, Lee BH (2009) Chilling stress-induced proteomic changes in rice roots. J Plant Physiol 166:1–11

    Article  CAS  PubMed  Google Scholar 

  • Leonardi GDA, Carlos NA, Mazzafera P, Balbuena TS (2015) Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genet Mol Biol 38:191–198

    Article  CAS  PubMed Central  Google Scholar 

  • Levi A, Panta GR, Parmentier CM, Muthalif MM, Arora R, Shanker S, Rowland LJ (1999) Complementary DNA cloning, sequencing and expression of an unusual dehydrin from blueberry floral buds. Physiol Plant 107:98–109

    Article  CAS  Google Scholar 

  • Li R, Wang C, Chen T, Chen P (2012) Quantitative proteomic analysis of cold-responsive proteins in Abelmoschus moschatus. J Anim Plant Sci 14:2006–2023

    Google Scholar 

  • Li L, Luo Z, Huang X, Zhang L, Zhao P, Ma H, Liu X (2015) Label-free quantitative proteomics to investigate strawberry fruit proteome changes under controlled atmosphere and low temperature storage. J Proteomics 120:44–57

    Article  CAS  PubMed  Google Scholar 

  • Liberek K, Lewandowska A, Zietkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27:328–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Beyer A, Aebersold R (2016a) On the dependency of cellular protein levels on mRNA abundance. Cell 165:535–550

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liang J, Sun L, Yang X, Li D (2016b) Group 3 LEA Protein, ZmLEA3, is involved in protection from low temperature stress. Front Plant Sci 7:1011

    PubMed  PubMed Central  Google Scholar 

  • Longo V, Kamran RV, Michaletti A, Toorchi M, Zolla L, Rinalducci S (2017) Proteomic and physiological response of spring barley leaves to cold stress. Cell 6:7

    Article  CAS  Google Scholar 

  • Lopez-Matas MA, Nuñez P, Soto A, Allona I, Casado R, Collada C, Gomez L (2004) Protein cryoprotective activity of a cytosolic small heat shock protein that accumulates constitutively in chestnut stems and is up-regulated by low and high temperatures. Plant Physiol 134:1708–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubaretz O, zur Nieden U (2002) Accumulation of plant small heat-stress proteins in storage organs. Planta 215:220–228

    Article  CAS  PubMed  Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–446

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maruyama K, Takeda M, Kidokoro S, Yamada K, Sakuma Y, Urano K, Sasaki R (2009) Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol 150:1972–1980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matros A, Kaspar S, Witzel K, Mock HP (2011) Recent progress in liquid chromatography-based separation and label-free quantitative plant proteomics. Phytochemistry 72:963–974

    Article  CAS  PubMed  Google Scholar 

  • McNeil PL (2002) Repairing a torn cell surface: make way, lysosomes to the rescue. J Cell Sci 115:873–879

    CAS  PubMed  Google Scholar 

  • Medina J, Bargues M, Terol J, Pe´rez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Zhao Q, Jin Y, Yu J, Yin Z, Chen S, Dai S (2016) Chilling-responsive mechanisms in halophyte Puccinellia tenuiflora seedlings revealed from proteomics analysis. J Proteomics 143:365–381

    Article  CAS  PubMed  Google Scholar 

  • Miller AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10:36–43

    Article  CAS  Google Scholar 

  • Minton K (2016) Gene expression: reading protein acetylation. Nat Rev Mol Cell Biol 17:676

    Article  CAS  PubMed  Google Scholar 

  • Mishra PK, Bisht SC, Bisht JK, Bhatt JC (2012) Cold-tolerant PGPRs as bioinoculants for stress management. Bacteria in agrobiology: stress management. Springer, Berlin, pp 95–118

    Chapter  Google Scholar 

  • Misra RC, Kamthan M, Kumar S, Ghosh S (2016) A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Sci Rep 6:25340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moghadam PK, Jackson MB (2013) The functional significance of synaptotagmin diversity in neuroendocrine secretion. Front Endocrinol 4:124

    Article  Google Scholar 

  • Mogk A, Schlieker C, Friedrich KL, Schönfeld HJ, Vierling E, Bukau B (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278:31033–31042

    Article  CAS  PubMed  Google Scholar 

  • Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP, Dhindsa RS (1993) A new cold-induced alfalfa gene is associated with enhanced hardening at subzero temperature. Plant Physiol 102:873–879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moura JCMS, Bonine CAV, De Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376

    Article  CAS  PubMed  Google Scholar 

  • Nadimpalli R, Yalpani N, Johal GS, Simmons CR (2000) Prohibitins, stomatins, and plant disease response genes comprise a protein superfamily that controls cell proliferation, ion channel regulation, and death. J Biol Chem 275:29579–29586

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Ishikawa M, Nakatani H, Oda A (2008) Characterization of cold responsive extracellular chitinase in bromegrass cell cultures and its relationship to antifreeze activity. Plant Physiol 147:391–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 144:513–523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama K, Okawa K, Kakizaki T, Inaba T (2014) Evaluation of the protective activities of a late embryogenesis abundant (LEA) related protein, Cor15am, during various stresses in vitro. Biosci Biotechnol Biochem 72:1642–1645

    Article  CAS  Google Scholar 

  • Neilson KA, Mariani M, Haynes PA (2011) Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics 11:1696–1706

    Article  PubMed  Google Scholar 

  • Neven LG, Haskell DW, Hofig A, Li QB, Guy CL (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21:291–305

    Article  CAS  PubMed  Google Scholar 

  • Nozu Y, Tsugita A, Kamijo K (2006) Proteomic analysis of rice leaf, stem and root tissues during growth course. Proteomics 6:3665–3670

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi S, Miyoshi T, Shirai S (2010) Low temperature stress at different flower developmental stages affects pollen development, pollination, and pod set in soybean. Environ Exp Bot 69:56–62

    Article  Google Scholar 

  • Ohta M, Takaiwa F (2014) Emerging features of ER resident J-proteins in plants. Plant Signal Behav 9:e28194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Dennis ES (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1551

    Article  CAS  Google Scholar 

  • Pandey A, Chakraborty S, Datta A, Chakraborty N (2008) Proteomics approach to identify dehydration responsive nuclear proteins from chickpea (Cicer arietinum L.). Mol Cell Proteomics 7:88–107

    Article  CAS  PubMed  Google Scholar 

  • Park CJ, Seo YS (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31(4):323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul S, Gayen D, Datta SK, Datta K (2015) Dissecting root proteome of transgenic rice cultivars unravels metabolic alterations and accumulation of novel stress responsive proteins under drought stress. Plant Sci 234:133–143

    Article  CAS  PubMed  Google Scholar 

  • Pedron L, Baldi P, Hietala AM, La Porta N (2009) Genotype-specific regulation of cold-responsive genes in cypress (Cupressus sempervirens L.). Gene 437:45–53

    Article  CAS  PubMed  Google Scholar 

  • Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijka KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petricka JJ, Schauer MA, Megraw M, Breakfield NW, Thompson JW, Georgiev S, Benfey PN (2012) The protein expression landscape of the Arabidopsis root. Proc Natl Acad Sci USA 109:6811–6818

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfannschmidt T, Ogrzewalla K, Baginsky S, Sickmann A, Meyer HE, Link G (2000) The multisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.). FEBS J 267:253–261

    CAS  Google Scholar 

  • Porat R, Pavoncello D, Lurie S, McCollum TG (2002) Identification of a grapefruit cDNA belonging to a unique class of citrus dehydrins and characterization of its expression patterns under temperature stress conditions. Physiol Plant 115:598–603

    Article  CAS  PubMed  Google Scholar 

  • Pradet A, Raymond P (1983) Adenine nucleotide ratios and adenylate energy charge in energy metabolism. Annu Rev Plant Biol 34:199–224

    Article  CAS  Google Scholar 

  • Pudney PDA, Buckley SL, Sidebottom CM, Twigg SN, Sevilla MP, Holt CB, Roper D, Telford JH et al (2003) The physio-chemical characterization of a boiling stable antifreeze protein from a perennial grass (Lolium perenne). Arch Biochem Biophys 410:238–245

    Article  CAS  PubMed  Google Scholar 

  • Puhakainen T, Li C, Malm MB, Kangasjarvi J, Heino P, Palva T (2004) Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor controlled gene during cold acclimation in silver birch. Plant Physiol 136:4299–4307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pya-Jones A (2011) Pre-mRNA splicing during transcription in the mammalian system. WIREs RNA 2:700–717

    Article  CAS  Google Scholar 

  • Pyee J, Kolattukudy PE (1995) The gene for the major cuticular wax-associated protein and three homologous genes from broccoli (Brassica oleracea) and their expression patterns. Plant J 7:49–59

    Article  CAS  PubMed  Google Scholar 

  • Pyee J, Yu H, Kolattukudy PE (1994) Identification of a lipid transfer protein as the major protein in the surface wax of broccoli (Brassica oleracea) leaves. Arch Biochem Biophys 311:460–468

    Article  CAS  PubMed  Google Scholar 

  • Qin G, Meng X, Wang Q, Tian S (2009) Oxidative damage of mitochondrial proteins contributes to fruit senescence: a redox proteomics analysis. J Proteome Res 8:2449–2462

    Article  CAS  PubMed  Google Scholar 

  • Qiu P (2003) Recent advances in computational promoter analysis in understanding the transcriptional regulatory network. Biochem Biophys Res Commun 309:495–501

    Article  CAS  PubMed  Google Scholar 

  • Raab S, Toth Z, de Groot C, Stamminger T, Hoth S (2006) ABA-responsive RNA-binding proteins are involved in chloroplast and stromule function in Arabidopsis seedlings. Planta 224:900–914

    Article  CAS  PubMed  Google Scholar 

  • Rappsilber J, Ryder U, Lamond AI, Mann M (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12:1231–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy A, Caler EV, Andrews NW (2001) Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes. Cell 106:157–169

    Article  CAS  PubMed  Google Scholar 

  • Renaut J, Hausman JF, Wisniewski ME (2006) Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109

    Article  CAS  Google Scholar 

  • Renaut J, Hausman JF, Bassett C, Artlip T, Cauchie HM, Witters E, Wisniewski M (2008) Quantitative proteomic analysis of short photoperiod and low-temperature responses in bark tissues of peach (Prunus persica L. Batsch). Tree Genet Genomes 4:589–600

    Article  Google Scholar 

  • Rodriguez EM, Svensson JT, Malatrasi M, Choi DW, Close TJ (2005) Barley Dhn13 encodes a KS-type dehydrin with constitutive and stress responsive expression. Theor Appl Genet 110:852–858

    Article  CAS  PubMed  Google Scholar 

  • Rodziewicz P, Swarcewicz B, Chmielewska K, Wojakowska A, Stobiecki M (2014) Influence of abiotic stresses on plant proteome and metabolome changes. Acta Physiol Plant 36:1–9

    Article  CAS  Google Scholar 

  • Rorat T, Grygorowicz WJ, Irzykowski W, Rey P (2004) Expression of KS-type dehydrins is primarily regulated by factor related to organ type and leaf developmental stage during vegetative growth. Planta 218:878–885

    Article  CAS  PubMed  Google Scholar 

  • Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148:635–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sage RF, McKown AD (2005) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J Exp Bot 57:303–317

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto H, Maruyama K, Sakuma Y, Meshi T, Iwabuchi M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Salekdeh GH, Komatsu S (2007) Crop proteomics: aim at sustainable agriculture of tomorrow. Proteomics 7:2976–2996

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Bel P, Egea I, Sanchez-Ballesta MT, Sevillano L, del Carmen Bolarin M, Flores FB (2012) Proteome changes in tomato fruits prior to visible symptoms of chilling injury are linked to defensive mechanisms, uncoupling of photosynthetic processes and protein degradation machinery. Plant Cell Physiol 53:470–484

    Article  CAS  PubMed  Google Scholar 

  • Sancho JP, Vanneste S, Lee E, McFarlane H, del Valle AE, Valpuesta V, Rosado A (2015) The Arabidopsis SYT1 is enriched in ER-PM contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168:132

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schurr U, Heckenberger U, Herdel K, Walter A, Feil R (2000) Leaf development in Ricinus communis during drought stress: dynamics of growth processes, of cellular structure and of sink–source transition. J Exp Bot 51:1515–1529

    Article  CAS  PubMed  Google Scholar 

  • Schwarzlander M, Fricker MD, Sweetlove LJ (2009) Monitoring the in vivo redox state of plant mitochondria: effect of respiratory inhibitors, abiotic stress and assessment of recovery from oxidative challenge. BBA-Bioenergetics 1787:468–475

    Article  CAS  PubMed  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Satou M (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Sergeant K, Kieffer P, Dommes J, Hausman JF, Renaut J (2014) Proteomic changes in leaves of poplar exposed to both cadmium and low-temperature. Environ Exp Bot 106:112–123

    Article  CAS  Google Scholar 

  • Shi J, Liu M, Chen Y, Wang J, Lu C (2016) Heterologous expression of the dehydrin-like protein gene AmCIP from Ammopiptanthus mongolicus enhances viability of Escherichia coli and tobacco under cold stress. Plant Growth Regul 79:71–80

    Article  CAS  Google Scholar 

  • Shimamura C, Ohno R, Nakamura C, Takumi S (2006) Improvement of freezing tolerance in tobacco plants expressing a cold-responsive and chloroplast-targeting protein WCOR15 of wheat. J Plant Physiol 163:213–219

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Sidebottom CS, Buckley P, Pudney S, Twigg C, Jarman C, Holt J, Telford A, McArthur D et al (2000) Heat-stable antifreeze protein from grass. Nature 406:256

    Article  CAS  PubMed  Google Scholar 

  • Simpson DJ, Smallwood M, Twigg S, Doucet CJ, Ross J, Bowles DJ (2005) Purification and characterization of an antifreeze protein from Forsythia suspensa (L.). Cryobiology 51:230–234

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Low ETL, Ooi LCL, Ong-Abdullah M, Nookiah R, Ting NC, Nagappan J (2014) The oil palm VIRESCENS gene controls fruit colour and encodes a R2R3-MYB. Nat Commun 5:4106

    Article  CAS  PubMed  Google Scholar 

  • Solecka D, Kacperska A (1993) Activity of l-phenylalanine ammonia-lyase in winter rape leaves treated with cold. Acta Biochim Pol 40:113–115

    CAS  PubMed  Google Scholar 

  • Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plant 119:253–262

    Article  CAS  Google Scholar 

  • Solecka D, Żebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants? Ann Bot 101:521–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spriggs KA, Bushell M, Willis AE (2010) Translational regulation of gene expression during conditions of cell stress. Mol Cell 40:228–237

    Article  CAS  PubMed  Google Scholar 

  • Strambio-De-Castillia C, Niepel M, Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11:490

    Article  CAS  PubMed  Google Scholar 

  • Subba P, Kumar R, Gayali S, Shekhar S, Parveen S, Pandey A, Chakraborty N (2013) Characterisation of the nuclear proteome of a dehydration-sensitive cultivar of chickpea and comparative proteomic analysis with a tolerant cultivar. Proteomics 13:1973–1992

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. BBA-Gene Struct Exp 1577:1–9

    Article  CAS  Google Scholar 

  • Sun J, Zheng T, Yu J, Wu T, Wang X, Chen G, Tian Y, Zhang H, Wang Y, Terzaghi W, Wang C (2017) TSV, a putative plastidic oxidoreductase, protects rice chloroplasts from cold stress during development by interacting with plastidic thioredoxin Z. New Phytol 215:240–255

    Article  CAS  PubMed  Google Scholar 

  • Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2013) Plant plasma membrane proteomics for improving cold tolerance. Front Plant Sci 4:90

    PubMed  PubMed Central  Google Scholar 

  • Takahashi D, Kawamura Y, Uemura M (2016) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. J Exp Bot 67:5203–5215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takuhara Y, Kobayashi M, Suzuki S (2011) Low-temperature-induced transcription factors in grapevine enhance cold tolerance in transgenic Arabidopsis plants. J Plant Physiol 168:967–975

    Article  CAS  PubMed  Google Scholar 

  • Takumi S, Nakamura C (2005) Abiotic stress signal pathways associated with development of freezing tolerance after cold acclimation in common wheat. Front Wheat Biosci 100:89–107

    Google Scholar 

  • Tan AS, Baty JW, Dong LF, Bezawork-Geleta A, Endaya B, Goodwin J, Pesdar EA (2015) Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA. Cell Metab 21:81–94

    Article  CAS  PubMed  Google Scholar 

  • Tanaka N, Mitsui S, Nobori H, Yanagi K, Komatsu S (2005) Expression and function of proteins during development of the basal region in rice seedlings. Mol Cell Proteomics 4:796–808

    Article  CAS  PubMed  Google Scholar 

  • Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics 4:1122–1133

    Article  CAS  PubMed  Google Scholar 

  • Taylor NL, Tan YF, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteomics 72:367–378

    Article  CAS  PubMed  Google Scholar 

  • Taylor NL, Heazlewood JL, Millar AH (2011) The Arabidopsis thaliana 2-D gel mitochondrial proteome: refining the value of reference maps for assessing protein abundance, contaminants and post-translational modifications. Proteomics 11:1720–1733

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tillemans V, Leponce I, Rausin G, Dispa L, Motte P (2006) Insights into nuclear organization in plants as revealed by the dynamic distribution of Arabidopsis SR splicing factors. Plant Cell 18:3218–3234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411

    Article  CAS  PubMed  Google Scholar 

  • Tomizioli M, Lazar C, Brugiere S, Burger T, Salvi D, Gatto L, Moyet L, Breckels LM, Hesse AM, Lilley KS, Seigneurin-Berny D (2014) Deciphering thylakoid sub-compartments using a mass spectrometry-based approach. Mol Cell Proteomics 28:114

    Google Scholar 

  • Touzet P, Meyer EH (2014) Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–171

    Article  CAS  PubMed  Google Scholar 

  • Uemura M, Steponkus PL (1997) Effect of cold acclimation on membrane lipid composition and freeze-induced membrane destablization. Plant cold hardiness. Springer, Boston, MA, pp 171–179

    Chapter  Google Scholar 

  • Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89

    Article  CAS  Google Scholar 

  • Ukaji N, Kuwabara C, Kanno Y, Seo M, Takezawa D, Arakawa K, Fujikawa S (2010) Endoplasmic reticulum-localized small heat shock protein that accumulates in mulberry tree (Morus bombycis Koidz.) during seasonal cold acclimation is responsive to abscisic acid. Tree Physiol 30:502–513

    Article  CAS  PubMed  Google Scholar 

  • Ullah H, Scappini EL, Moon AF, Williams LV, Armstrong DL, Pedersen LC (2008) Structure of a signal transduction regulator, RACK1, from Arabidopsis thaliana. Protein Sci 17:1771–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valentim-Neto PA, Rossi GB, Anacleto KB, de Mello CS, Balsamo GM, Arisi ACM (2016) Leaf proteome comparison of two GM common bean varieties and their non-GM counterparts by principal component analysis. J Sci Food Agric 96:927–932

    Article  CAS  PubMed  Google Scholar 

  • Van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155:1578–1588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanderschuren H, Lentz E, Zainuddin I, Gruissem W (2013) Proteomics of model and crop plant species: status, current limitations and strategic advances for crop improvement. J Proteomics 93:5–19

    Article  CAS  PubMed  Google Scholar 

  • Vega-García MO, López-Espinoza G, Ontiveros JC, Caro-Corrales JJ, Vargas FD, López-Valenzuela JA (2010) Changes in protein expression associated with chilling injury in tomato fruit. J Am Soc Hortic Sci 135:83–89

    Article  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  PubMed  Google Scholar 

  • Vogel JP, Raab TK, Somerville CR, Somerville SC (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J 40:968–978

    Article  CAS  PubMed  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Yang P, Zhang X, Xu Y, Kuang T, Shen S, He Y (2009) Proteomic analysis of the cold stress response in the moss, Physcomitrella patens. Proteomics 9:4529–4538

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Fang G, Li Y, Ding M, Gong H, Li Y (2013) Differential antioxidant responses to cold stress in cell suspension cultures of two subspecies of rice. Plant Cell Tissue Organ Cult 113:353–361

    Article  CAS  Google Scholar 

  • Wang S, Zhang G, Zhang Y, Song Q, Chen Z, Wang J, Ma S (2015) Comparative studies of mitochondrial proteomics reveal an intimate protein network of male sterility in wheat (Triticum aestivum L.). J Exp Bot 66:6191–6203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wani MA, Jan N, Qazi HA, Andrabi KI, John R (2018) Cold stress induces biochemical changes, fatty acid profile, anti-oxidant system and gene expression in Capsella bursa pastoris L. Acta Physiol Plant 40:167

    Article  CAS  Google Scholar 

  • Weckwerth P, Ehlert B, Romeis T (2015) ZmCPK1, a calcium-independent kinase member of the Zea mays CDPK gene family, functions as a negative regulator in cold stress signalling. Plant Cell Environ 38:544–558

    Article  CAS  PubMed  Google Scholar 

  • Wellin BV, Olson A, Nylander M, Palva ET (1994) Characterization and differential expression of Dhn/Lea/Rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144

    Article  Google Scholar 

  • Wen X, Wang S, Duman JG, Arifin JF, Juwita V, Goddard WA, Rios A, Liu F, Kim SK, Abrol R, DeVries AL, Henling LM (2016) Antifreeze proteins govern the precipitation of trehalose in a freezing-avoiding insect at low temperature. Proc Natl Acad Sci 113(24):6683–6688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wisniewski M, Webb R, Balsamo R, Close TJ, Yu XM, Griffith M (1999) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600–608

    Article  CAS  Google Scholar 

  • Wu FZ, Wang BC, Yang CP (2014) Proteomic analysis of the cold stress response in the leaves of birch (Betula platyphylla Suk). Plant Omics 7:195

    Google Scholar 

  • Xu J, Li Y, Sun J, Du L, Zhang Y, Yu Q, Liu X (2013) Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biol 15:292–303

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Yang Y, Xie L, Li X, Feng C et al (2014) Involvement of multiple types of dehydrins in the freezing response in loquat (Eriobotrya japonica). PLoS ONE 9:e87575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xuan J, Song Y, Zhang H, Liu J, Guo Z, Hua Y (2013) Comparative proteomic analysis of the stolon cold stress response between the C4 perennial grass species Zoysia japonica and Zoysia metrella. PLoS ONE 8:e75705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389–3404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 5:484–496

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Schuster G, Stern DB (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell 8:1409–1420

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang XH, Xu ZH, Xue HW (2005) Arabidopsis membrane steroid binding protein 1 is involved in inhibition of cell elongation. Plant Cell 17:116–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang W, Zhang L, Lv H, Li H, Zhang Y, Xu Y (2015) The K-segments of wheat dehydrin WZY2 are essential for its protective functions under temperature stress. Front Plant Sci 6:406

    PubMed  PubMed Central  Google Scholar 

  • Yao K, Lockhart KM, Kalanack JJ (2005) Cloning of dehydrin sequences from Brassica juncea and Brassica napus and their low temperature-inducible expression in germinating seeds. Plant Physiol Biochem 43:83–89

    Article  CAS  PubMed  Google Scholar 

  • Yin G, Sun H, Xin X, Qin G, Liang Z, Jing X (2009) Mitochondrial damage in the soybean seed axis during imbibition at chilling temperatures. Plant Cell Physiol 50:1305–1318

    Article  CAS  PubMed  Google Scholar 

  • Yokota H, Iehisa JC, Shimosaka E, Takumi S (2015) Line differences in Cor/Lea and fructan biosynthesis-related gene transcript accumulation are related to distinct freezing tolerance levels in synthetic wheat hexaploids. J Plant Physiol 176:78–88

    Article  CAS  PubMed  Google Scholar 

  • Yokotani N, Sato Y, Tanabe S, Chujo T, Shimizu T, Okada K, Kaku H (2013) WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance. J Exp Bot 64:5085–5097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon GM, Kieber JJ (2013) 14-3-3 regulates 1-aminocyclopropane-1-carboxylate synthase protein turnover in Arabidopsis. Plant Cell 25:1016–1028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126:1232–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F, Shao X, Yu L, Xu F, Wang H (2015) Proteomic analysis of postharvest peach fruit subjected to chilling stress or non-chilling stress temperatures during storage. Sci Hortic 197:72–89

    Article  CAS  Google Scholar 

  • Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279

    Article  CAS  PubMed  Google Scholar 

  • Zargar SM, Mahajan R, Nazir M, Nagar P, Kim ST, Rai V, Agrawal GK (2017) Common bean proteomics: present status and future strategies. J Proteomics 169:239–248

    Article  CAS  PubMed  Google Scholar 

  • Zhang SH, Wei YL, Liu J, Yu HM, Yin JH, Pan HY, Baldwin TC (2011) An apoplastic chitinase CpCHT1 isolated from the corolla of wintersweet exhibits both antifreeze and antifungal activities. Biol Plant 55:141–148

    Article  CAS  Google Scholar 

  • Zhang S, Guoqi SONG, Yulian LI, Jie GAO, Jiao WANG, Guiju CHEN, Zhendong ZHAO (2014) Comparative proteomic analysis of cold responsive proteins in two wheat cultivars with different tolerance to spring radiation frost. Front Agric Sci Eng 1:37–45

    Article  Google Scholar 

  • Zhang W, Zhang H, Ning L, Li B, Bao M (2016) Quantitative proteomic analysis provides novel insights into cold stress responses in Petunia seedlings. Front Plant Sci 7:136

    PubMed  PubMed Central  Google Scholar 

  • Zhao C, Zhang Z, Xie S, Si T, Li Y, Zhu JK (2016) Mutational evidence for the critical role of CBF genes in cold acclimation in Arabidopsis. Plant Physiol 171:2744

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng M, Wang Y, Liu K, Shu H, Zhou Z (2012) Protein expression changes during cotton fiber elongation in response to low temperature stress. J Plant Physiol 169:399–409

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Chen S, Alvarez S, Asirvatham VS, Schachtman DP, Wu Y, Sharp RE (2006) Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol 140:311–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Biochem 68:118–126

    Article  CAS  PubMed  Google Scholar 

  • Zoschke R, Bock R (2018) Chloroplast translation: structural and functional organization, operational control, and regulation. Plant Cell 30:745–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS ONE 3:e1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support by Department of Biotechnology and Department of Science and Technology, Govt. India. DBT and DST, Govt. of India.

Author information

Authors and Affiliations

  1. Plant Molecular Biology Laboratory, Department of Botany, University of Kashmir, Srinagar, Kashmir, 190 006, India

    Nelofer Jan, Hilal Ahmad Qazi, Vaseem Raja & Riffat John

Authors
  1. Nelofer Jan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hilal Ahmad Qazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vaseem Raja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Riffat John
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Riffat John.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jan, N., Qazi, H.A., Raja, V. et al. Proteomics: A tool to decipher cold tolerance. Theor. Exp. Plant Physiol. 31, 183–213 (2019). https://doi.org/10.1007/s40626-019-00140-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40626-019-00140-2

Keywords

Search

Navigation