Proteomics: A tool to decipher cold tolerance
- 15 Downloads
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.
Keywords
Proteomics Cold stress Cold tolerance Plant antifreeze proteinsAbbreviations
- 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
Notes
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.
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 30:745–763CrossRefPubMedGoogle 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 57:509–517CrossRefGoogle Scholar
- Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889CrossRefPubMedGoogle 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 23:2499–2513CrossRefPubMedPubMedCentralGoogle 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 170:864–873CrossRefPubMedGoogle 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 57:1537–1546CrossRefPubMedGoogle 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 282:9260–9268CrossRefGoogle 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 92:9353–9357CrossRefPubMedGoogle 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 34:1095–1110CrossRefPubMedPubMedCentralGoogle 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 12:1–11CrossRefGoogle 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 33:61–70CrossRefPubMedGoogle 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 3:16006CrossRefGoogle 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 93:13404–13409CrossRefPubMedGoogle Scholar
- Atıcı Ö, Nalbantoǧlu B (2003) Antifreeze proteins in higher plants. Phytochemistry 64:1187–1196CrossRefPubMedGoogle Scholar
- Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543CrossRefPubMedGoogle 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 171:389–398CrossRefPubMedGoogle 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 71:315–324CrossRefPubMedGoogle Scholar
- Bae MS, Cho EJ, Choi EY, Park OK (2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. Plant J 36:652–663CrossRefPubMedGoogle 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 24:701–713CrossRefPubMedGoogle 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 202:1320–1334CrossRefPubMedGoogle Scholar
- Battaglia M, Covarrubias AA (2013) Late embryogenesis abundant (LEA) proteins in legumes. Front Plant Sci 4:190CrossRefPubMedPubMedCentralGoogle 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 16:65CrossRefPubMedPubMedCentralGoogle Scholar
- Bishop RE (2000) The bacterial lipocalins. BBA-Protein Struct Molecular Enzymol 1482:73–83CrossRefGoogle Scholar
- Bosl B, Grimminger V, Walter S (2006) The molecular chaperone Hsp104-a molecular machine for protein disaggregation. J Struct Biol 156:139–148CrossRefPubMedGoogle 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 118:262–269CrossRefGoogle 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)):D233-8PubMedGoogle 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 14:2723–2744CrossRefPubMedGoogle 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 CrossRefGoogle Scholar
- Chen L, Madura K (2002) Rad23 promotes the targeting of proteolytic substrates to the proteasome. Mol Cell Biol 22:4902–4913CrossRefPubMedPubMedCentralGoogle 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 5:194Google 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 1819:120–128Google 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 6:105PubMedPubMedCentralGoogle 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 8:264–265Google 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 54:1075–1083CrossRefPubMedGoogle 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 62:93–100CrossRefGoogle 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 5:3162–3172CrossRefPubMedGoogle 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 10:623–638CrossRefPubMedPubMedCentralGoogle Scholar
- Die JV, Arora R, Rowland LJ (2016) Global patterns of protein abundance during the development of cold hardiness in blueberry. Environ Exp Bot 124:11–21CrossRefGoogle 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 85:51–61CrossRefPubMedGoogle 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 129:1368–1381CrossRefGoogle Scholar
- Douce R (2012) Mitochondria in higher plants: structure, function, and biogenesis. Elsevier, AmsterdamGoogle Scholar
- Duman JG (1994) Purification and characterization of a thermal hysteresis protein from a plant, the bittersweet nightshade Solanum dulcamara. Biochim Biophys Acta 1206:129–135CrossRefPubMedGoogle 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 180:86–98CrossRefPubMedGoogle Scholar
- Dundr M, Misteli T (2002) Nucleolomics: an inventory of the nucleolus. Mol Cell 9:5–7CrossRefPubMedGoogle 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 14:1557–1566CrossRefPubMedPubMedCentralGoogle 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 137:391–399Google 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 78:503–514CrossRefPubMedGoogle 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 21:296–301CrossRefGoogle 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 38:179–190CrossRefGoogle 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 140:214–222Google 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 98:99–111CrossRefGoogle 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 14:1675–1690CrossRefPubMedPubMedCentralGoogle 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 127:1676–1681CrossRefPubMedPubMedCentralGoogle Scholar
- Fox AH, Lam YW, Leung AK, Lyon CE, Andersen J, Mann M, Lamond AI (2002) Paraspeckles: a novel nuclear domain. Curr Biol 12:13–25CrossRefPubMedGoogle 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 17:283CrossRefPubMedPubMedCentralGoogle 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 10:3001–3019CrossRefPubMedGoogle 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 230:1033–1046CrossRefPubMedGoogle 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 27:476CrossRefGoogle Scholar
- Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82:331–371CrossRefPubMedGoogle 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 41:3897–3905CrossRefPubMedGoogle Scholar
- Ghosh D, Xu J (2014) Abiotic stress responses in plant roots: a proteomics perspective. Front Plant Sci 5:6CrossRefPubMedPubMedCentralGoogle Scholar
- Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle 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 16:433–442CrossRefPubMedGoogle Scholar
- Gokirmak T, Paul AL, Ferl RJ (2010) Plant phosphopeptide-binding proteins as signaling mediators. Curr Opin Plant Biol 13:527–532CrossRefPubMedGoogle 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 14:447–457CrossRefPubMedGoogle 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 47:720–734CrossRefPubMedGoogle 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 7:901CrossRefPubMedPubMedCentralGoogle Scholar
- Graether SP, Boddington KF (2014) Disorder and function: a review of the dehydrin protein family. Front Plant Sci 5:576CrossRefPubMedPubMedCentralGoogle Scholar
- Griffith M, Yaish MW (2004) Antifreeze proteins in overwintering plants: a tale of two activities. Trends Plant Sci 9:399–405CrossRefPubMedGoogle Scholar
- Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG (2005) Antifreeze proteins modify the freezing process in planta. Plant Physiol 138:330–340CrossRefPubMedPubMedCentralGoogle 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 10:506–516CrossRefPubMedGoogle 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 8:71CrossRefPubMedPubMedCentralGoogle Scholar
- Guimil S, Dunand C (2007) Cell growth and differentiation in Arabidopsis epidermal cells. J Exp Bot 58:3829–3840CrossRefPubMedGoogle Scholar
- Guo W, Ward RW, Thomashow MF (1992) Characterization of a cold-regulated wheat gene related to Arabidopsis Cor47. Plant Physiol 100:915–922CrossRefPubMedPubMedCentralGoogle 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 155:370–383CrossRefPubMedGoogle 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 48:1775–1782CrossRefGoogle 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 11:2684–2696CrossRefPubMedGoogle Scholar
- Gupta R, Deswal R (2014) Antifreeze proteins enable plants to survive in freezing conditions. J Biosci 39:931–944CrossRefPubMedGoogle Scholar
- Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384CrossRefPubMedGoogle 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 130:639–648CrossRefPubMedPubMedCentralGoogle Scholar
- Han R, Campbell KP (2007) Dysferlin and muscle membrane repair. Curr Opin Cell Biol 19:409–416CrossRefPubMedPubMedCentralGoogle 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 63:236–244CrossRefPubMedGoogle 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 6:1503–1509CrossRefPubMedPubMedCentralGoogle Scholar
- Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112CrossRefPubMedPubMedCentralGoogle Scholar
- Hara M (2010) The multifunctionality of dehydrins: an overview. Plant Signal Behav 5:503–508CrossRefPubMedGoogle 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 217:290–298PubMedGoogle Scholar
- Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662CrossRefPubMedGoogle Scholar
- Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703CrossRefPubMedGoogle Scholar
- Harholt J, Suttangkakul A, Scheller HV (2010) Biosynthesis of pectin. Plant Physiol 153:384–395CrossRefPubMedPubMedCentralGoogle Scholar
- Hashimoto M, Komatsu S (2007) Proteomic analysis of rice seedlings during cold stress. Proteomics 7:1293–1302CrossRefPubMedGoogle 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 16:685–697CrossRefPubMedGoogle Scholar
- Heidarvand L, Maali-Amiri R (2013) Physio-biochemical and proteome analysis of chickpea in early phases of cold stress. J Plant Physiol 170:459–469CrossRefPubMedGoogle 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 57:3601–3618CrossRefPubMedGoogle 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 47–54CrossRefGoogle 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 264:241–250CrossRefPubMedGoogle 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 109:879–889CrossRefPubMedPubMedCentralGoogle Scholar
- Hossain Z, Hajika M, Komatsu S (2012) Comparative proteome analysis of high and low cadmium accumulating soybeans under cadmium stress. Amino Acids 43:2393–2416CrossRefPubMedGoogle 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 2:381–387CrossRefPubMedGoogle 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 48:339–350CrossRefPubMedGoogle 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 11:264CrossRefPubMedPubMedCentralGoogle 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 207–239CrossRefGoogle 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 124:81–95CrossRefGoogle Scholar
- Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47:291–305CrossRefGoogle Scholar
- Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118CrossRefPubMedPubMedCentralGoogle 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 5:274–292CrossRefPubMedGoogle 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 96:13566–13570CrossRefPubMedGoogle 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 115:1287–1289CrossRefGoogle Scholar
- Jacoby RP, Millar AH, Taylor NL (2010) Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J Proteome Res 9:6595–6604CrossRefPubMedGoogle Scholar
- Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106CrossRefPubMedGoogle 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 109:19–31CrossRefGoogle 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 YorkGoogle Scholar
- Jan N, Wani UM, Andrabi KI, John R (2018b) Cold stress modulates osmolytes and antioxidant system in Calendula officinalis. Acta Physiol Plant 40:73CrossRefGoogle Scholar
- Janmohammadi M, Mock HP, Matros A (2014) Proteomic analysis of cold acclimation in winter wheat under field conditions. Icel Agric Sci 27:3–15Google Scholar
- Janmohammadi M, Zolla L, Rinalducci S (2015) Low temperature tolerance in plants: changes at the protein level. Phytochemistry 117:76–89CrossRefPubMedGoogle Scholar
- Janska A, Marsík P, Zelenková S, Ovesna J (2010) Cold stress and acclimation—what is important for metabolic adjustment? Plant Biol 12:395–405CrossRefPubMedGoogle 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 11:307–325CrossRefPubMedPubMedCentralGoogle 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 203:776–789CrossRefGoogle Scholar
- Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14:787–802CrossRefPubMedGoogle Scholar
- Jarzabeck M, Pukacki PM, Nuc K (2009) Cold-regulated proteins with potent antifreeze and cryoprotective activities in spruces (Picea spp.). Cryobiology 58:268–274CrossRefGoogle Scholar
- Ji L, Zhou P, Zhu Y, Liu F, Li R, Qiu Y (2017) Proteomic analysis of rice seedlings under cold stress. Protein J 36:299–307CrossRefPubMedGoogle 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 10:18991–19004CrossRefGoogle Scholar
- John R, Anjum NA, Sopory SK, Akram NA, Ashraf M (2016) Some key physiological and molecular processes of cold acclimation. Biol Plant 60:603–618CrossRefGoogle 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 49:128–158CrossRefGoogle 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 255:59–71CrossRefPubMedGoogle Scholar
- Kader JC (1997) Lipid-transfer proteins: a puzzling family of plant proteins. Trends Plant Sci 2:66–70CrossRefGoogle Scholar
- Kampinga HH, Craig EA (2010) The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat Rev 11:579–592CrossRefGoogle 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 122:31–39CrossRefPubMedGoogle 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 85:769–777CrossRefGoogle Scholar
- Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154CrossRefPubMedGoogle Scholar
- Kazuoka T, Oeda K (1992) Heat-stable COR (cold-regulated) proteins associated with freezing tolerance in spinach [Spinacia oleracea]. Plant Cell Physiol 33:1107–1114Google 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:e0138010CrossRefPubMedPubMedCentralGoogle Scholar
- King HA, Gerber AP (2014) Translatome profiling: methods for genome-scale analysis of mRNA translation. Brief Funct Genomics 15:22–31PubMedGoogle 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 57:315–332CrossRefPubMedGoogle 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 35:225–231PubMedGoogle 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 159:1787–1805CrossRefPubMedPubMedCentralGoogle 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) 79:102–110CrossRefGoogle Scholar
- Komatsu S, Yanagawa Y (2013) Cell wall proteomics of crops. Front Plant Sci 4:17PubMedPubMedCentralGoogle 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 277:713CrossRefPubMedGoogle 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 31:139–160CrossRefGoogle 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 34:405–418Google 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 60:3595–3609CrossRefPubMedGoogle Scholar
- Kosová K, Vítámvás P, Prášil IT (2007) The role of dehydrins in plant response to cold. Biol Plant 51:601–617CrossRefGoogle 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 74:1301–1322CrossRefPubMedGoogle 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 9:122CrossRefPubMedPubMedCentralGoogle Scholar
- Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiol 155:70–78CrossRefPubMedGoogle Scholar
- Larance M, Lamond AI (2015) Multidimensional proteomics for cell biology. Nat Rev Mol Cell Biol 16:269CrossRefPubMedGoogle 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 57:104–112CrossRefPubMedGoogle 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 87:1–15CrossRefPubMedGoogle 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 19:212–218PubMedGoogle 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 62:151–164CrossRefPubMedGoogle 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 166:1–11CrossRefPubMedGoogle Scholar
- Leonardi GDA, Carlos NA, Mazzafera P, Balbuena TS (2015) Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genet Mol Biol 38:191–198CrossRefPubMedCentralGoogle 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 107:98–109CrossRefGoogle Scholar
- Li R, Wang C, Chen T, Chen P (2012) Quantitative proteomic analysis of cold-responsive proteins in Abelmoschus moschatus. J Anim Plant Sci 14:2006–2023Google 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 120:44–57CrossRefPubMedGoogle Scholar
- Liberek K, Lewandowska A, Zietkiewicz S (2008) Chaperones in control of protein disaggregation. EMBO J 27:328–335CrossRefPubMedPubMedCentralGoogle 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 10:1391–1406CrossRefPubMedPubMedCentralGoogle Scholar
- Liu Y, Beyer A, Aebersold R (2016a) On the dependency of cellular protein levels on mRNA abundance. Cell 165:535–550CrossRefPubMedGoogle 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 7:1011PubMedPubMedCentralGoogle 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 6:7CrossRefGoogle 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 134:1708–1717CrossRefPubMedPubMedCentralGoogle Scholar
- Lubaretz O, zur Nieden U (2002) Accumulation of plant small heat-stress proteins in storage organs. Planta 215:220–228CrossRefPubMedGoogle Scholar
- Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Physiol 24:445–446CrossRefGoogle 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 38:982–993CrossRefPubMedGoogle 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 150:1972–1980CrossRefPubMedPubMedCentralGoogle Scholar
- Matros A, Kaspar S, Witzel K, Mock HP (2011) Recent progress in liquid chromatography-based separation and label-free quantitative plant proteomics. Phytochemistry 72:963–974CrossRefPubMedGoogle Scholar
- McNeil PL (2002) Repairing a torn cell surface: make way, lysosomes to the rescue. J Cell Sci 115:873–879PubMedGoogle 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 119:463–469CrossRefPubMedPubMedCentralGoogle 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 143:365–381CrossRefPubMedGoogle Scholar
- Miller AH, Heazlewood JL, Kristensen BK, Braun HP, Moller IM (2005) The plant mitochondrial proteome. Trends Plant Sci 10:36–43CrossRefGoogle Scholar
- Minton K (2016) Gene expression: reading protein acetylation. Nat Rev Mol Cell Biol 17:676CrossRefPubMedGoogle 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 95–118CrossRefGoogle 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 6:25340CrossRefPubMedPubMedCentralGoogle Scholar
- Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337CrossRefPubMedPubMedCentralGoogle Scholar
- Moghadam PK, Jackson MB (2013) The functional significance of synaptotagmin diversity in neuroendocrine secretion. Front Endocrinol 4:124CrossRefGoogle 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 278:31033–31042CrossRefPubMedGoogle 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 102:873–879CrossRefPubMedPubMedCentralGoogle 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 52:360–376CrossRefPubMedGoogle 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 275:29579–29586CrossRefPubMedGoogle 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 147:391–401CrossRefPubMedPubMedCentralGoogle Scholar
- Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432CrossRefPubMedPubMedCentralGoogle 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 144:513–523CrossRefPubMedPubMedCentralGoogle 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 72:1642–1645CrossRefGoogle Scholar
- Neilson KA, Mariani M, Haynes PA (2011) Quantitative proteomic analysis of cold-responsive proteins in rice. Proteomics 11:1696–1706CrossRefPubMedGoogle 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 21:291–305CrossRefPubMedGoogle Scholar
- Nozu Y, Tsugita A, Kamijo K (2006) Proteomic analysis of rice leaf, stem and root tissues during growth course. Proteomics 6:3665–3670CrossRefPubMedGoogle 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 69:56–62CrossRefGoogle Scholar
- Ohta M, Takaiwa F (2014) Emerging features of ER resident J-proteins in plants. Plant Signal Behav 9:e28194CrossRefPubMedPubMedCentralGoogle 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 28:1534–1551CrossRefGoogle 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 7:88–107CrossRefPubMedGoogle Scholar
- Park CJ, Seo YS (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31(4):323CrossRefPubMedPubMedCentralGoogle 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 234:133–143CrossRefPubMedGoogle Scholar
- Pedron L, Baldi P, Hietala AM, La Porta N (2009) Genotype-specific regulation of cold-responsive genes in cypress (Cupressus sempervirens L.). Gene 437:45–53CrossRefPubMedGoogle 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 12:319–341CrossRefPubMedPubMedCentralGoogle 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 109:6811–6818CrossRefPubMedGoogle 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 267:253–261Google 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 115:598–603CrossRefPubMedGoogle Scholar
- Pradet A, Raymond P (1983) Adenine nucleotide ratios and adenylate energy charge in energy metabolism. Annu Rev Plant Biol 34:199–224CrossRefGoogle 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 410:238–245CrossRefPubMedGoogle 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 136:4299–4307CrossRefPubMedPubMedCentralGoogle Scholar
- Pya-Jones A (2011) Pre-mRNA splicing during transcription in the mammalian system. WIREs RNA 2:700–717CrossRefGoogle 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 7:49–59CrossRefPubMedGoogle 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 311:460–468CrossRefPubMedGoogle 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 8:2449–2462CrossRefPubMedGoogle Scholar
- Qiu P (2003) Recent advances in computational promoter analysis in understanding the transcriptional regulatory network. Biochem Biophys Res Commun 309:495–501CrossRefPubMedGoogle 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 224:900–914CrossRefPubMedGoogle Scholar
- Rappsilber J, Ryder U, Lamond AI, Mann M (2002) Large-scale proteomic analysis of the human spliceosome. Genome Res 12:1231–1245CrossRefPubMedPubMedCentralGoogle Scholar
- Reddy A, Caler EV, Andrews NW (2001) Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes. Cell 106:157–169CrossRefPubMedGoogle Scholar
- Renaut J, Hausman JF, Wisniewski ME (2006) Proteomics and low-temperature studies: bridging the gap between gene expression and metabolism. Physiol Plant 126:97–109CrossRefGoogle 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 4:589–600CrossRefGoogle 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 110:852–858CrossRefPubMedGoogle 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 36:1–9CrossRefGoogle 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 218:878–885CrossRefPubMedGoogle 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 148:635–652CrossRefPubMedPubMedCentralGoogle Scholar
- Sage RF, McKown AD (2005) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J Exp Bot 57:303–317CrossRefPubMedGoogle 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 136:2734–2746CrossRefPubMedPubMedCentralGoogle 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 290:998–1009CrossRefPubMedGoogle Scholar
- Salekdeh GH, Komatsu S (2007) Crop proteomics: aim at sustainable agriculture of tomorrow. Proteomics 7:2976–2996CrossRefPubMedGoogle 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 53:470–484CrossRefPubMedGoogle 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 168:132CrossRefGoogle Scholar
- Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12:30CrossRefPubMedPubMedCentralGoogle 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 51:1515–1529CrossRefPubMedGoogle 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 1787:468–475CrossRefPubMedGoogle 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 31:279–292CrossRefPubMedGoogle 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 106:112–123CrossRefGoogle 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 79:71–80CrossRefGoogle 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 163:213–219CrossRefPubMedGoogle 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 6:410–417CrossRefPubMedGoogle 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 406:256CrossRefPubMedGoogle 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 51:230–234CrossRefPubMedGoogle 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 5:4106CrossRefPubMedPubMedCentralGoogle Scholar
- Solecka D, Kacperska A (1993) Activity of l-phenylalanine ammonia-lyase in winter rape leaves treated with cold. Acta Biochim Pol 40:113–115PubMedGoogle Scholar
- Solecka D, Kacperska A (2003) Phenylpropanoid deficiency affects the course of plant acclimation to cold. Physiol Plant 119:253–262CrossRefGoogle 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 101:521–530CrossRefPubMedPubMedCentralGoogle Scholar
- Spriggs KA, Bushell M, Willis AE (2010) Translational regulation of gene expression during conditions of cell stress. Mol Cell 40:228–237CrossRefPubMedGoogle 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 11:490CrossRefPubMedGoogle 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 13:1973–1992CrossRefPubMedGoogle Scholar
- Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. BBA-Gene Struct Exp 1577:1–9CrossRefGoogle 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 215:240–255CrossRefPubMedGoogle Scholar
- Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2013) Plant plasma membrane proteomics for improving cold tolerance. Front Plant Sci 4:90PubMedPubMedCentralGoogle 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 67:5203–5215CrossRefPubMedPubMedCentralGoogle 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 168:967–975CrossRefPubMedGoogle 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 100:89–107Google 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 21:81–94CrossRefPubMedPubMedCentralGoogle 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 4:796–808CrossRefPubMedGoogle Scholar
- Taylor NL, Heazlewood JL, Day DA, Millar AH (2005) Differential impact of environmental stresses on the pea mitochondrial proteome. Mol Cell Proteomics 4:1122–1133CrossRefPubMedGoogle 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 72:367–378CrossRefPubMedGoogle 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 11:1720–1733CrossRefPubMedGoogle Scholar
- Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8CrossRefPubMedPubMedCentralGoogle 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 18:3218–3234CrossRefPubMedPubMedCentralGoogle Scholar
- Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Proteomics 71:391–411CrossRefPubMedGoogle 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 28:114Google Scholar
- Touzet P, Meyer EH (2014) Cytoplasmic male sterility and mitochondrial metabolism in plants. Mitochondrion 19:166–171CrossRefPubMedGoogle 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 171–179CrossRefGoogle Scholar
- Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89CrossRefGoogle 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 30:502–513CrossRefPubMedGoogle 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 17:1771–1780CrossRefPubMedPubMedCentralGoogle 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 96:927–932CrossRefPubMedGoogle Scholar
- Van Wijk KJ, Baginsky S (2011) Plastid proteomics in higher plants: current state and future goals. Plant Physiol 155:1578–1588CrossRefPubMedPubMedCentralGoogle 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 93:5–19CrossRefPubMedGoogle 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 135:83–89Google Scholar
- Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132CrossRefPubMedGoogle 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 40:968–978CrossRefPubMedGoogle 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 41:195–211CrossRefPubMedGoogle 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 9:4529–4538CrossRefPubMedGoogle 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 113:353–361CrossRefGoogle 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 66:6191–6203CrossRefPubMedPubMedCentralGoogle 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 40:167CrossRefGoogle 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 38:544–558CrossRefPubMedGoogle 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 26:131–144CrossRefGoogle 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):6683–6688CrossRefPubMedGoogle 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 105:600–608CrossRefGoogle 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 7:195Google 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 15:292–303CrossRefPubMedGoogle 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:e87575CrossRefPubMedPubMedCentralGoogle 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:e75705CrossRefPubMedPubMedCentralGoogle 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 6:251–264CrossRefPubMedPubMedCentralGoogle Scholar
- Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803CrossRefPubMedGoogle Scholar
- Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:3389–3404CrossRefPubMedPubMedCentralGoogle 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 5:484–496CrossRefPubMedGoogle Scholar
- Yang J, Schuster G, Stern DB (1996) CSP41, a sequence-specific chloroplast mRNA binding protein, is an endoribonuclease. Plant Cell 8:1409–1420CrossRefPubMedPubMedCentralGoogle Scholar
- Yang XH, Xu ZH, Xue HW (2005) Arabidopsis membrane steroid binding protein 1 is involved in inhibition of cell elongation. Plant Cell 17:116–131CrossRefPubMedPubMedCentralGoogle 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 6:406PubMedPubMedCentralGoogle 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 43:83–89CrossRefPubMedGoogle 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 50:1305–1318CrossRefPubMedGoogle 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 176:78–88CrossRefPubMedGoogle 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 64:5085–5097CrossRefPubMedPubMedCentralGoogle Scholar
- Yoon GM, Kieber JJ (2013) 14-3-3 regulates 1-aminocyclopropane-1-carboxylate synthase protein turnover in Arabidopsis. Plant Cell 25:1016–1028CrossRefPubMedPubMedCentralGoogle Scholar
- Yu XM, Griffith M, Wiseman SB (2001) Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol 126:1232–1240CrossRefPubMedPubMedCentralGoogle 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 197:72–89CrossRefGoogle Scholar
- Zachariassen KE, Kristiansen E (2000) Ice nucleation and antinucleation in nature. Cryobiology 41:257–279CrossRefPubMedGoogle 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 169:239–248CrossRefPubMedGoogle 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 55:141–148CrossRefGoogle 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 1:37–45CrossRefGoogle 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 7:136PubMedPubMedCentralGoogle 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 171:2744PubMedPubMedCentralGoogle 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 169:399–409CrossRefPubMedGoogle Scholar
- Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedPubMedCentralGoogle 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 140:311–325CrossRefPubMedPubMedCentralGoogle 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 10:290–295CrossRefPubMedGoogle 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 68:118–126CrossRefPubMedGoogle Scholar
- Zoschke R, Bock R (2018) Chloroplast translation: structural and functional organization, operational control, and regulation. Plant Cell 30:745–770CrossRefPubMedPubMedCentralGoogle 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:e1994CrossRefPubMedPubMedCentralGoogle Scholar