Biological Networks Underlying Abiotic Stress Tolerance in Temperate Crops--A Proteomic Perspective
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
26340626
PubMed Central
PMC4613235
DOI
10.3390/ijms160920913
PII: ijms160920913
Knihovny.cz E-zdroje
- Klíčová slova
- abiotic stresses, multiple stress, protein functions, protein markers, proteomics, stress tolerance, temperate crops,
- MeSH
- biologická adaptace * genetika MeSH
- biologické markery MeSH
- fyziologický stres * genetika MeSH
- genotyp MeSH
- proteom * MeSH
- proteomika * metody MeSH
- rostlinné proteiny genetika metabolismus MeSH
- zemědělské plodiny genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- biologické markery MeSH
- proteom * MeSH
- rostlinné proteiny MeSH
Abiotic stress factors, especially low temperatures, drought, and salinity, represent the major constraints limiting agricultural production in temperate climate. Under the conditions of global climate change, the risk of damaging effects of abiotic stresses on crop production increases. Plant stress response represents an active process aimed at an establishment of novel homeostasis under altered environmental conditions. Proteins play a crucial role in plant stress response since they are directly involved in shaping the final phenotype. In the review, results of proteomic studies focused on stress response of major crops grown in temperate climate including cereals: common wheat (Triticum aestivum), durum wheat (Triticum durum), barley (Hordeum vulgare), maize (Zea mays); leguminous plants: alfalfa (Medicago sativa), soybean (Glycine max), common bean (Phaseolus vulgaris), pea (Pisum sativum); oilseed rape (Brassica napus); potato (Solanum tuberosum); tobacco (Nicotiana tabaccum); tomato (Lycopersicon esculentum); and others, to a wide range of abiotic stresses (cold, drought, salinity, heat, imbalances in mineral nutrition and heavy metals) are summarized. The dynamics of changes in various protein functional groups including signaling and regulatory proteins, transcription factors, proteins involved in protein metabolism, amino acid metabolism, metabolism of several stress-related compounds, proteins with chaperone and protective functions as well as structural proteins (cell wall components, cytoskeleton) are briefly overviewed. Attention is paid to the differences found between differentially tolerant genotypes. In addition, proteomic studies aimed at proteomic investigation of multiple stress factors are discussed. In conclusion, contribution of proteomic studies to understanding the complexity of crop response to abiotic stresses as well as possibilities to identify and utilize protein markers in crop breeding processes are discussed.
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Temperate Climate. [(accessed on 13 May 2015)]. Available online: http://en.wikipedia.org/w/index.php?title=Temperate_climate&oldid=654335237.
Kosová K., Prášil I.T. Annual Field Crops. In: Storey K.B., Tanino K.K., editors. Temperature Adaptation in a Changing Climate: Nature at Risk. CAB International; Wallingford, UK: 2012. pp. 186–207.
Levitt J. Responses of Plants to Environmental Stresses. Volume 1. Academic Publisher; New York, NY, USA: 1980. p. 497.
Larcher W. Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups. 4th ed. Springer Science & Business Media; Heidelberg, Germany: 2003. p. 513.
Kosová K., Vítámvás P., Prášil I.T., Renaut J. Plant proteome changes under abiotic stress—Contribution of proteomics studies to understanding plant stress response. J. Proteom. 2011;74:1301–1322. doi: 10.1016/j.jprot.2011.02.006. PubMed DOI
Salekdeh G.H., Komatsu S. Crop proteomics: Aim at sustainable agriculture of tomorrow. Proteomics. 2007;7:2976–2996. doi: 10.1002/pmic.200700181. PubMed DOI
Zhang H., Han B., Wang T., Chen S., Li H., Zhang Y., Dai S. Mechanisms of plant salt response: Insights from proteomics. J. Proteome Res. 2012;11:49–67. doi: 10.1021/pr200861w. PubMed DOI
Kosová K., Prášil I.T., Vítámvás P. Protein contribution to plant salinity response and tolerance acquisition. Int. J. Mol. Sci. 2013;14:6757–6789. doi: 10.3390/ijms14046757. PubMed DOI PMC
Kosová K., Vítámvás P., Urban M.O., Prášil I.T. Plant proteome responses to salinity stress—Comparison of glycophytes and halophytes. Funct. Plant Biol. 2013;40:775–786. PubMed
Hossain Z., Nouri M.-Z., Komatsu S. Plant cell organelle proteomics in response to abiotic stress. J. Proteome Res. 2012;11:37–48. doi: 10.1021/pr200863r. PubMed DOI
Ahsan N., Renaut J., Komatsu S. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics. 2009;9:2602–2621. doi: 10.1002/pmic.200800935. PubMed DOI
Komatsu S., Kamal A.H.M., Hossain Z. Wheat proteomics: Proteome modulation and abiotic stress acclimation. Front. Plant Sci. 2014;5:684. doi: 10.3389/fpls.2014.00684. PubMed DOI PMC
Kosová K., Vítámvás P., Prášil I.T. Proteomics of stress responses in wheat and barley-search for potential protein markers of stress tolerance. Front. Plant Sci. 2014;5:711. doi: 10.3389/fpls.2014.00711. PubMed DOI PMC
Komatsu S., Ahsan N. Soybean proteomics and its application to functional analysis. J. Proteom. 2009;72:325–336. doi: 10.1016/j.jprot.2008.10.001. PubMed DOI
Komatsu S., Sakata K., Nanjo Y. “Omics” techniques and their use to identify how soybean responds to flooding. J. Anal. Sci. Technol. 2015;6:9. doi: 10.1186/s40543-015-0052-7. DOI
FAO: 2013. [(accessed on 14 April 2015)]. Available online: http://faostat3.fao.org/browse/rankings/commodities_by_regions/E.
Schnable P.S., Ware D., Fulton R.S., Stein J.C., Wei F., Pasternak S., Liang C., Zhang J., Fulton L., Graves T.A., et al. The b73 maize genome: Complexity, diversity, and dynamics. Science. 2009;326:1112–1115. doi: 10.1126/science.1178534. PubMed DOI
Xu X., Pan S., Cheng S., Zhang B., Mu D., Ni P., Zhang G., Yang S., Li R., Wang J., et al. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475:U189–U194. doi: 10.1038/nature10158. PubMed DOI
Mayer K.F.X., Waugh R., Langridge P., Close T.J., Wise R.P., Graner A., Matsumoto T., Sato K., Schulman A., Muehlbauer G.J., et al. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491:711–716. doi: 10.1038/nature11543. PubMed DOI
Eversole K., Feuillet C., Mayer K.F.X., Rogers J. Slicing the wheat genome. Science. 2014;345:285–285. doi: 10.1126/science.1257983. PubMed DOI
Schmutz J., Cannon S.B., Schlueter J., Ma J., Mitros T., Nelson W., Hyten D.L., Song Q., Thelen J.J., Cheng J., et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463:178–183. doi: 10.1038/nature08670. PubMed DOI
Schmutz J., McClean P.E., Mamidi S., Wu G.A., Cannon S.B., Grimwood J., Jenkins J., Shu S., Song Q., Chavarro C., et al. A reference genome for common bean and genome-wide analysis of dual domestications. Nat. Genet. 2014;46:707–713. doi: 10.1038/ng.3008. PubMed DOI PMC
Sierro N., Battey J.N.D., Ouadi S., Bakaher N., Bovet L., Willig A., Goepfert S., Peitsch M.C., Ivanov N.V. The tobacco genome sequence and its comparison with those of tomato and potato. Nat. Commun. 2014;5:3833. doi: 10.1038/ncomms4833. PubMed DOI PMC
Sato S., Tabata S., Hirakawa H., Asamizu E., Shirasawa K., Isobe S., Kaneko T., Nakamura Y., Shibata D., Aoki K., et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485:635–641. doi: 10.1038/nature11119. PubMed DOI PMC
Chalhoub B., Denoeud F., Liu S., Parkin I.A.P., Tang H., Wang X., Chiquet J., Belcram H., Tong C., Samans B., et al. Early allopolyploid evolution in the post-neolithic Brassica napus oilseed genome. Science. 2014;345:950–953. doi: 10.1126/science.1253435. PubMed DOI
Dohm J.C., Minoche A.E., Holtgraewe D., Capella-Gutierrez S., Zakrzewski F., Tafer H., Rupp O., Sørensen T., Stracke R., Reinhardt R., et al. The genome of the recently domesticated crop plant sugar beet (Beta vulgaris) Nature. 2014;505:546–549. doi: 10.1038/nature12817. PubMed DOI
Guo S., Zhang J., Sun H., Salse J., Lucas W.J., Zhang H., Zheng Y., Mao L., Ren Y., Wang Z., et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 2013;45:51–58. doi: 10.1038/ng.2470. PubMed DOI
Jaillon O., Aury J.-M., Noel B., Policriti A., Clepet C., Casagrande A., Choisne N., Aubourg S., Vitulo N., Jubin C., et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449:463–467. doi: 10.1038/nature06148. PubMed DOI
Caruso G., Cavaliere C., Guarino C., Gubbiotti R., Foglia P., Laganà A. Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass spectrometry. Anal. Bioanal. Chem. 2008;391:381–390. doi: 10.1007/s00216-008-2008-x. PubMed DOI
Caruso G., Cavaliere C., Foglia P., Gubbiotti R., Samperi R., Laganà A. Analysis of drought responsive proteins in wheat (Triticum durum) by 2D-PAGE and MALDI-TOF mass spectrometry. Plant Sci. 2009;177:570–576. doi: 10.1016/j.plantsci.2009.08.007. DOI
Alvarez S., Berla B.M., Sheffield J., Cahoon R.E., Jez J.M., Hicks L.M. Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics. 2009;9:2419–2431. doi: 10.1002/pmic.200800478. PubMed DOI
Balbuena T.S., Salas J.J., Martinez-Force E., Garces R., Thelen J.J. Proteome analysis of cold acclimation in sunflower. J. Proteome Res. 2011;10:2330–2346. doi: 10.1021/pr101137q. PubMed DOI
Ghaffari M., Toorchi M., Valizadeh M., Komatsu S. Differential response of root proteome to drought stress in drought sensitive and tolerant sunflower inbred lines. Funct. Plant Biol. 2013;40:609–617. doi: 10.1071/FP12251. PubMed DOI
Hradilová J., Řehulka P., Řehulková H., Vrbová M., Griga M., Brzobohatý B. Comparative analysis of proteomic changes in contrasting flax cultivars upon cadmium exposure. Electrophoresis. 2010;31:421–431. doi: 10.1002/elps.200900477. PubMed DOI
Klubicová K., Danchenko M., Skultéty L., Berezhna V.V., Hricová A., Rashydav N.M., Hajduch M. Agricultural recovery of a formerly radioactive area: II. Systematic proteomic characterization of flax seed development in the remediated chernobyl area. J. Proteom. 2011;74:1378–1384. doi: 10.1016/j.jprot.2011.02.029. PubMed DOI
Aranjuelo I., Molero G., Erice G., Christophe Avice J., Nogues S. Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.) J. Exp. Bot. 2011;62:111–123. doi: 10.1093/jxb/erq249. PubMed DOI PMC
Li G., Peng X., Xuan H., Wei L., Yang Y., Guo T., Kang G. Proteomic analysis of leaves and roots of common wheat (Triticum aestivum L.) under copper-stress conditions. J. Proteome Res. 2013;12:4846–4861. doi: 10.1021/pr4008283. PubMed DOI
Li W., Wei Z., Qiao Z., Wu Z., Cheng L., Wang Y. Proteomics analysis of alfalfa response to heat stress. PLoS ONE. 2013;8:e82725. doi: 10.1371/journal.pone.0082725. PubMed DOI PMC
Alves M., Francisco R., Martins I., Ricardo C.P.P. Analysis of Lupinus albus leaf apoplastic proteins in response to boron deficiency. Plant Soil. 2006;279:1–11. doi: 10.1007/s11104-005-3154-y. DOI
Degand H., Faber A.-M., Dauchot N., Mingeot D., Watillon B., van Cutsem P., Morsomme P., Boutry M. Proteomic analysis of chicory root identifies proteins typically involved in cold acclimation. Proteomics. 2009;9:2903–2907. doi: 10.1002/pmic.200800744. PubMed DOI
Kav N.N.V., Srivastava S., Goonewardene L., Blade S.F. Proteome-level changes in the roots of Pisum sativum in response to salinity. Ann. Appl. Biol. 2004;145:217–230. doi: 10.1111/j.1744-7348.2004.tb00378.x. DOI
Taylor N.L., Heazlewood J.L., Day D.A., Millar A.H. Differential impact of environmental stresses on the pea mitochondrial proteome. Mol. Cell. Proteom. 2005;4:1122–1133. doi: 10.1074/mcp.M400210-MCP200. PubMed DOI
Murata N., Los D.A. Membrane fluidity and temperature perception. Plant Physiol. 1997;115:875–879. PubMed PMC
Suzuki I., Los D.A., Kanesaki Y., Mikami K., Murata N. The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J. 2000;19:1327–1334. doi: 10.1093/emboj/19.6.1327. PubMed DOI PMC
Zhu J.K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 2002;53:247–273. doi: 10.1146/annurev.arplant.53.091401.143329. PubMed DOI PMC
Munns R. Genes and salt tolerance: Bringing them together. New Phytol. 2005;167:645–663. doi: 10.1111/j.1469-8137.2005.01487.x. PubMed DOI
Peng Z., Wang M., Li F., Lv H., Li C., Xia G. A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol. Cell. Proteom. 2009;8:2676–2686. doi: 10.1074/mcp.M900052-MCP200. PubMed DOI PMC
Zörb C., Herbst R., Forreiter C., Schubert S. Short-term effects of salt exposure on the maize chloroplast protein pattern. Proteomics. 2009;9:4209–4220. doi: 10.1002/pmic.200800791. PubMed DOI
Zörb C., Schmitt S., Mühling K.H. Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics. 2010;10:4441–4449. doi: 10.1002/pmic.201000231. PubMed DOI
Nouri M.-Z., Komatsu S. Comparative analysis of soybean plasma membrane proteins under osmotic stress using gel-based and LC MS/MS-based proteomics approaches. Proteomics. 2010;10:1930–1945. doi: 10.1002/pmic.200900632. PubMed DOI
Zhang M., Lv D., Ge P., Bian Y., Chen G., Zhu G., Li X., Yan Y. Phosphoproteome analysis reveals new drought response and defense mechanisms of seedling leaves in bread wheat (Triticum aestivum L.) J. Proteom. 2014;109:290–308. doi: 10.1016/j.jprot.2014.07.010. PubMed DOI
Yang Z.-B., Eticha D., Fuehrs H., Heintz D., Ayoub D., Van Dorsselaer A., Schlingmann B., Rao I.M., Braun H.-P., Horst W.J. Proteomic and phosphoproteomic analysis of polyethylene glycol-induced osmotic stress in root tips of common bean (Phaseolus vulgaris L.) J. Exp. Bot. 2013;64:5569–5586. doi: 10.1093/jxb/ert328. PubMed DOI PMC
Denison F.C., Paul A.-L., Zupanska A.K., Ferl R.J. 14-3-3 proteins in plant physiology. Sem. Cell Dev. Biol. 2011;22:720–727. doi: 10.1016/j.semcdb.2011.08.006. PubMed DOI
Wang M.-C., Peng Z.-Y., Li C.-L., Li F., Liu C., Xia G.-M. Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics. 2008;8:1470–1489. doi: 10.1002/pmic.200700569. PubMed DOI
Kang G., Li G., Xu W., Peng X., Han Q., Zhu Y., Guo T. Proteomics reveals the effects of salicylic acid on growth and tolerance to subsequent drought stress in wheat. J. Proteome Res. 2012;11:6066–6079. doi: 10.1021/pr300728y. PubMed DOI
Ghabooli M., Khatabi B., Ahmadi F.S., Sepehri M., Mirzaei M., Amirkhani A., Jorrin-Novo J.V., Salekdeh G.H. Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J. Proteom. 2013;94:289–301. doi: 10.1016/j.jprot.2013.09.017. PubMed DOI
Alvarez S., Choudhury S.R., Pandey S. Comparative quantitative proteomics analysis of the ABA response of roots of drought-sensitive and drought-tolerant wheat varieties identifies proteomic signatures of drought adaptability. J. Proteome Res. 2014;13:1688–1701. doi: 10.1021/pr401165b. PubMed DOI
Guo G., Ge P., Ma C., Li X., Lv D., Wang S., Ma W., Yan Y. Comparative proteomic analysis of salt response proteins in seedling roots of two wheat varieties. J. Proteom. 2012;75:1867–1885. doi: 10.1016/j.jprot.2011.12.032. PubMed DOI
Wendelboe-Nelson C., Morris P.C. Proteins linked to drought tolerance revealed by DIGE analysis of drought resistant and susceptible barley varieties. Proteomics. 2012;12:3374–3385. doi: 10.1002/pmic.201200154. PubMed DOI
Rinalducci S., Egidi M.G., Karimzadeh G., Jazii F.R., Zolla L. Proteomic analysis of a spring wheat cultivar in response to prolonged cold stress. Electrophoresis. 2011;32:1807–1818. doi: 10.1002/elps.201000663. PubMed DOI
Rinalducci S., Egidi M.G., Mahfoozi S., Godehkahriz S.J., Zolla L. The influence of temperature on plant development in a vernalization-requiring winter wheat: A 2-DE based proteomic investigation. J. Proteom. 2011;74:643–659. doi: 10.1016/j.jprot.2011.02.005. PubMed DOI
Kosová K., Vítámvás P., Planchon S., Renaut J., Vaňková R., Prášil I.T. Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. J. Proteome Res. 2013;12:4830–4845. doi: 10.1021/pr400600g. PubMed DOI
Kosová K., Vítámvás P., Prášilová P., Prášil I.T. Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale. Biol. Plant. 2013;57:105–112. doi: 10.1007/s10535-012-0237-5. DOI
Aghaei K., Ehsanpour A.A., Shah A.H., Komatsu S. Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids. 2009;36:91–98. doi: 10.1007/s00726-008-0036-7. PubMed DOI
Yong W.D., Xu Y.Y., Xu W.Z., Wang X., Li N., Wu J.S., Liang T.B., Chong K., Xu Z.H., Tan K.H., et al. Vernalization-induced flowering in wheat is mediated by a lectin-like gene VER2. Planta. 2003;217:261–270. PubMed
Vincent D., Ergul A., Bohlman M.C., Tattersall E.A.R., Tillett R.L., Wheatley M.D., Woolsey R., Quilici D.R., Joets J., Schlauch K., et al. Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J. Exp. Bot. 2007;58:1873–1892. doi: 10.1093/jxb/erm012. PubMed DOI
Bandehagh A., Salekdeh G.H., Toorchi M., Mohammadi A., Komatsu S. Comparative proteomic analysis of canola leaves under salinity stress. Proteomics. 2011;11:1965–1975. doi: 10.1002/pmic.201000564. PubMed DOI
Thompson J.E., Hopkins M.T., Taylor C., Wang T.W. Regulation of senescence by eukaryotic translation initiation factor 5A: Implications for plant growth and development. Trends Plant Sci. 2004;9:174–179. doi: 10.1016/j.tplants.2004.02.008. PubMed DOI
Sarhadi E., Mahfoozi S., Hosseini S.A., Salekdeh G.H. Cold acclimation proteome analysis reveals close link between the up-regulation of low-temperature associated proteins and vernalization fulfillment. J. Proteome Res. 2010;9:5658–5667. doi: 10.1021/pr100475r. PubMed DOI
Han Q., Kang G., Guo T. Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum) Plant Physiol. Biochem. 2013;63:236–244. doi: 10.1016/j.plaphy.2012.12.002. PubMed DOI
Hoepflinger M.C., Reitsamer J., Geretschlaeger A.M., Mehlmer N., Tenhaken R. The effect of translationally controlled tumour protein (TCTP) on programmed cell death in plants. BMC Plant Biol. 2013;13:135. doi: 10.1186/1471-2229-13-135. PubMed DOI PMC
Mostek A., Börner A., Badowiec A., Weidner S. Alterations in root proteome of salt-sensitive and tolerant barley lines under salt stress conditions. J. Plant Physiol. 2015;174:166–176. doi: 10.1016/j.jplph.2014.08.020. PubMed DOI
Fercha A., Capriotti A.L., Caruso G., Cavaliere C., Gherroucha H., Samperi R., Stampachiacchiere S., Laganà A. Gel-free proteomics reveal potential biomarkers of priming-induced salt tolerance in durum wheat. J. Proteom. 2013;91:486–499. doi: 10.1016/j.jprot.2013.08.010. PubMed DOI
Alam I., Sharmin S.A., Kim K.-H., Yang J.K., Choi M.S., Lee B.H. Proteome analysis of soybean roots subjected to short-term drought stress. Plant Soil. 2010;333:491–505. doi: 10.1007/s11104-010-0365-7. DOI
Vítámvás P., Prášil I.T., Kosová K., Planchon S., Renaut J. Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics. 2012;12:68–85. doi: 10.1002/pmic.201000779. PubMed DOI
Fatehi F., Hosseinzadeh A., Alizadeh H., Brimavandi T., Struik P.C. The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Mol. Biol. Rep. 2012;39:6387–6397. doi: 10.1007/s11033-012-1460-z. PubMed DOI
Rasoulnia A., Bihamta M.R., Peyghambari S.A., Alizadeh H., Rahnama A. Proteomic response of barley leaves to salinity. Mol. Biol. Rep. 2011;38:5055–5063. doi: 10.1007/s11033-010-0651-8. PubMed DOI
Oh M., Komatsu S. Characterization of proteins in soybean roots under flooding and drought stresses. J. Proteom. 2015;114:161–181. doi: 10.1016/j.jprot.2014.11.008. PubMed DOI
Patterson J., Ford K., Cassin A., Natera S., Bacic A. Increased abundance of proteins involved in phytosiderophore production in boron-tolerant barley. Plant Physiol. 2007;144:1612–1631. doi: 10.1104/pp.107.096388. PubMed DOI PMC
Witzel K., Weidner A., Surabhi G.-K., Börner A., Mock H.-P. Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J. Exp. Bot. 2009;60:3545–3557. doi: 10.1093/jxb/erp198. PubMed DOI PMC
Gao L., Yan X., Li X., Guo G., Hu Y., Ma W., Yan Y. Proteome analysis of wheat leaf under salt stress by two-dimensional difference gel electrophoresis (2D-DIGE) Phytochemistry. 2011;72:1180–1191. doi: 10.1016/j.phytochem.2010.12.008. PubMed DOI
Hajheidari M., Abdollahian-Noghabi M., Askari H., Heidari M., Sadeghian S.Y., Ober E.S., Salekdeh G.H. Proteome analysis of sugar beet leaves under drought stress. Proteomics. 2005;5:950–960. doi: 10.1002/pmic.200401101. PubMed DOI
Vítámvás P., Urban M.O., Škodáček Z., Kosová K., Pitelková I., Vítámvás J., Renaut J., Prášil I.T. Quantitative analysis of proteome extracted from barley crowns grown under different drought conditions. Front. Plant Sci. 2015;6:479. doi: 10.3389/fpls.2015.00479. PubMed DOI PMC
Tai F.J., Yuan Z.L., Wu X.L., Zhao P.F., Hu X.L., Wang W. Identification of membrane proteins in maize leaves, altered in expression under drought stress through polyethylene glycol treatment. Plant Omics J. 2011;4:250–256.
Kamal A.H.M., Cho K., Kim D.-E., Uozumi N., Chung K.-Y., Lee S.Y., Choi J.-S., Cho S.-W., Shin C.-S., Woo S.H. Changes in physiology and protein abundance in salt-stressed wheat chloroplasts. Mol. Biol. Rep. 2012;39:9059–9074. doi: 10.1007/s11033-012-1777-7. PubMed DOI
Ashoub A., Beckhaus T., Berberich T., Karas M., Brueggemann W. Comparative analysis of barley leaf proteome as affected by drought stress. Planta. 2013;237:771–781. doi: 10.1007/s00425-012-1798-4. PubMed DOI
Ye J., Wang S., Zhang F., Xie D., Yao Y. Proteomic analysis of leaves of different wheat genotypes subjected to PEG 6000 stress and rewatering. Plant Omics J. 2013;6:286–294.
Faghani E., Gharechahi J., Komatsu S., Mirzaei M., Khavarinejad R.A., Najafi F., Farsad L.K., Salekdeh G.H. Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. J. Proteom. 2015;114:1–15. doi: 10.1016/j.jprot.2014.10.018. PubMed DOI
Bazargani M.M., Sarhadi E., Bushehri A.-A.S., Matros A., Mock H.-P., Naghavi M.-R., Hajihoseini V., Mardi M., Hajirezaei M.-R., Moradi F., et al. A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J. Proteom. 2011;74:1959–1973. doi: 10.1016/j.jprot.2011.05.015. PubMed DOI
Bahrman N., Le Gouis J., Negroni L., Amilhat L., Leroy P., Lainé A.L., Jaminon O. Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. Proteomics. 2004;4:709–719. doi: 10.1002/pmic.200300571. PubMed DOI
Rollins J.A., Habte E., Templer S.E., Colby T., Schmidt J., von Korff M. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.) J. Exp. Bot. 2013;64:3201–3212. doi: 10.1093/jxb/ert158. PubMed DOI PMC
Razavizadeh R., Ehsanpour A.A., Ahsan N., Komatsu S. Proteome analysis of tobacco leaves under salt stress. Peptides. 2009;30:1651–1659. doi: 10.1016/j.peptides.2009.06.023. PubMed DOI
Aghaei K., Ehsanpour A.A., Komatsu S. Proteome analysis of potato under salt stress. J. Proteome Res. 2008;7:4858–4868. doi: 10.1021/pr800460y. PubMed DOI
Kausar R., Arshad M., Shahzad A., Komatsu S. Proteomics analysis of sensitive and tolerant barley genotypes under drought stress. Amino Acids. 2013;44:345–359. doi: 10.1007/s00726-012-1338-3. PubMed DOI
Sobhanian H., Razavizadeh R., Nanjo Y., Ehsanpour A.A., Jazii F.R., Motamed N., Komatsu S. Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Sci. 2010;8:19. doi: 10.1186/1477-5956-8-19. PubMed DOI PMC
Budak H., Akpinar B.A., Unver T., Turktas M. Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI-MS/MS. Plant Mol. Biol. 2013;83:89–103. doi: 10.1007/s11103-013-0024-5. PubMed DOI
Xu J., Li Y., Sun J., Du L., Zhang Y., Yu Q., Liu X. Comparative physiological and proteomic response to abrupt low temperature stress between two winter wheat cultivars differing in low temperature tolerance. Plant Biol. 2013;15:292–303. doi: 10.1111/j.1438-8677.2012.00639.x. PubMed DOI
Jacoby R.P., Millar A.H., Taylor N.L. Wheat mitochondrial proteomes provide new links between antioxidant defense and plant salinity tolerance. J. Proteome Res. 2010;9:6595–6604. doi: 10.1021/pr1007834. PubMed DOI
Jacoby R.P., Millar A.H., Taylor N.L. Investigating the role of respiration in plant salinity tolerance by analyzing mitochondrial proteomes from wheat and a salinity-tolerant amphiploid (wheat × Lophopyrum elongatum) J. Proteome Res. 2013;12:4807–4829. doi: 10.1021/pr400504a. PubMed DOI
Yu F., Han X., Geng C., Zhao Y., Zhang Z., Qiu F. Comparative proteomic analysis revealing the complex network associated with waterlogging stress in maize (Zea mays L.) seedling root cells. Proteomics. 2015;15:135–147. doi: 10.1002/pmic.201400156. PubMed DOI
Gharechahi J., Alizadeh H., Naghavi M.R., Sharifi G. A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.) Mol. Biol. Rep. 2014;41:3897–3905. doi: 10.1007/s11033-014-3257-8. PubMed DOI
Lee H., Guo Y., Ohta M., Xiong L.M., Stevenson B., Zhu J.K. LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J. 2002;21:2692–2702. doi: 10.1093/emboj/21.11.2692. PubMed DOI PMC
Singh R., Green M.R. Sequence-specific binding of transfer-RNA by glyceraldehyde-3-phosphate dehydrogenase. Science. 1993;259:365–368. doi: 10.1126/science.8420004. PubMed DOI
Sirover M.A. New insights into an old protein: The functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim. Biophys. Acta. 1999;1432:159–184. doi: 10.1016/S0167-4838(99)00119-3. PubMed DOI
Hajheidari M., Eivazi A., Buchanan B.B., Wong J.H., Majidi I., Salekdeh G.H. Proteomics uncovers a role for redox in drought tolerance in wheat. J. Proteome Res. 2007;6:1451–1460. doi: 10.1021/pr060570j. PubMed DOI
Houde M., Danyluk J., Laliberte J.F., Rassart E., Dhindsa R.S., Sarhan F. Cloning, characterization, and expression of a carrier DNA encoding a 50-kD protein specifically induced by cold-acclimation in wheat. Plant Physiol. 1992;99:1381–1387. doi: 10.1104/pp.99.4.1381. PubMed DOI PMC
Brini F., Hanin M., Lumbreras V., Irar S., Pagés M., Masmoudi K. Functional characterization of DHN-5, a dehydrin showing a differential phosphorylation pattern in two Tunisian durum wheat (Triticum durum Desf.) varieties with marked differences in salt and drought tolerance. Plant. Sci. 2007;172:20–28. doi: 10.1016/j.plantsci.2006.07.011. DOI
Kosová K., Holková L., Prášil I.T., Prášilová P., Bradáčová M., Vítámvás P., Čapková V. Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare) J. Plant Physiol. 2008;165:1142–1151. doi: 10.1016/j.jplph.2007.10.009. PubMed DOI
Vítámvás P., Saalbach G., Prášil I.T., Čapková V., Opatrná J., Ahmed J. WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J. Plant Physiol. 2007;164:1197–1207. doi: 10.1016/j.jplph.2006.06.011. PubMed DOI
Crosatti C., Soncini C., Stanca A.M., Cattivelli L. The accumulation of a cold-regulated chloroplastic protein is light-dependent. Planta. 1995;196:458–463. doi: 10.1007/BF00203644. PubMed DOI
Vágújfalvi A., Crosatti C., Galiba G., Dubcovský J., Cattivelli L. Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the COR14b gene in frost-tolerant and frost-sensitive genotypes. Mol. Gen. Genet. 2000;263:194–200. PubMed
Vágújfalvi A., Galiba G., Cattivelli L., Dubcovský J. The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr.-A2 on wheat chromosome 5A. Mol. Gen. Genom. 2003;269:60–67. PubMed PMC
Skylas D.J., Cordwell S.J., Hains P.G., Larsen M.R., Basseal D.J., Walsh B.J., Blumenthal C., Rathmell W., Copeland L., Wrigley C.W. Heat shock of wheat during grain filling: Proteins associated with heat-tolerance. J. Cereal Sci. 2002;35:175–188. doi: 10.1006/jcrs.2001.0410. DOI
Majoul T., Bancel E., Triboi E., Ben Hamida J., Branlard G. Proteomic analysis of the effect of heat stress on hexaploid wheat grain: Characterization of heat-responsive proteins from non-prolamins fraction. Proteomics. 2004;4:505–513. doi: 10.1002/pmic.200300570. PubMed DOI
Kawasaki S., Miyake C., Kohchi T., Fujii S., Uchida M., Yokota A. Responses of wild watermelon to drought stress: Accumulation of an ArgE homologue and citrulline in leaves during water deficits. Plant Cell Physiol. 2000;41:864–873. doi: 10.1093/pcp/pcd005. PubMed DOI
Ahsan N., Lee D.-G., Lee S.-H., Kang K.Y., Bahk J.D., Choi M.S., Lee I.-J., Renaut J., Lee B.-H. A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol. Plant. 2007;131:555–570. doi: 10.1111/j.1399-3054.2007.00980.x. PubMed DOI
Benešová M., Holá D., Fischer L., Jedelský P.L., Hnilička F., Wilhelmová N., Rothová O., Kočová M., Procházková D., Honnerová J., et al. The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS ONE. 2012;7:e38017. doi: 10.1371/journal.pone.0038017. PubMed DOI PMC
Hlaváčková I., Vítámvás P., Šantrůček J., Kosová K., Zelenková S., Prášil I.T., Ovesná J., Hynek R., Kodíček M. Proteins involved in distinct phases of cold hardening process in frost resistant winter barley (Hordeum vulgare L.) cv Luxor. Int. J. Mol. Sci. 2013;14:8000–8024. doi: 10.3390/ijms14048000. PubMed DOI PMC
Riccardi F., Gazeau P., Jacquemot M.P., Vincent D., Zivy M. Deciphering genetic variations of proteome responses to water deficit in maize leaves. Plant Physiol. Biochem. 2004;42:1003–1011. doi: 10.1016/j.plaphy.2004.09.009. PubMed DOI
Ge P., Ma C., Wang S., Gao L., Li X., Guo G., Ma W., Yan Y. Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal. Bioanal. Chem. 2012;402:1297–1313. doi: 10.1007/s00216-011-5532-z. PubMed DOI
Fercha A., Capriotti A.L., Caruso G., Caualiere C., Samperi R., Stampachiacchiere S., Laganà A. Comparative analysis of metabolic proteome variation in ascorbate-primed and unprimed wheat seeds during germination under salt stress. J. Proteom. 2014;108:238–257. doi: 10.1016/j.jprot.2014.04.040. PubMed DOI
Guo S., Wharton W., Moseley P., Shi H. Heat shock protein 70 regulates cellular redox status by modulating glutathione-related enzyme activities. Cell Stress Chaperones. 2007;12:245–254. doi: 10.1379/CSC-265.1. PubMed DOI PMC
Komatsu S., Kobayashi Y., Nishizawa K., Nanjo Y., Furukawa K. Comparative proteomics analysis of differentially expressed proteins in soybean cell wall during flooding stress. Amino Acids. 2010;39:1435–1449. doi: 10.1007/s00726-010-0608-1. PubMed DOI
Manaa A., Ben Ahmed H., Valot B., Bouchet J.-P., Aschi-Smiti S., Causse M., Faurobert M. Salt and genotype impact on plant physiology and root proteome variations in tomato. J. Exp. Bot. 2011;62:2797–2813. doi: 10.1093/jxb/erq460. PubMed DOI
Dixon D.P., Skipsey M., Edwards R. Roles for glutathione transferases in plant secondary metabolism. Phytochemistry. 2010;71:338–350. doi: 10.1016/j.phytochem.2009.12.012. PubMed DOI
Edreva A. Pathogenesis-related proteins: Research progress in the last 15 years. Gen. Appl. Plant Physiol. 2005;31:105–124.
Jellouli N., Ben Jouira H., Skouri H., Ghorbel A., Gourgouri A., Mliki A. Proteomic analysis of Tunisian grapevine cultivar Razegui under salt stress. J. Plant Physiol. 2008;165:471–481. doi: 10.1016/j.jplph.2007.02.009. PubMed DOI
Sugimoto M., Takeda K. Proteomic analysis of specific proteins in the root of salt-tolerant barley. Biosci. Biotechnol. Biochem. 2009;73:2762–2765. doi: 10.1271/bbb.90456. PubMed DOI
Dani V., Simon W.J., Duranti M., Croy R.R.D. Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics. 2005;5:737–745. doi: 10.1002/pmic.200401119. PubMed DOI
Witzel K., Matros A., Strickert M., Kaspar S., Peukert M., Mühling K.H., Börner A., Mock H.-P. Salinity stress in roots of contrasting barley genotypes reveals time-distinct and genotype-specific patterns for defined proteins. Mol. Plant. 2014;7:336–355. doi: 10.1093/mp/sst063. PubMed DOI
Dao T.T.H., Linthorst H.J.M., Verpoorte R. Chalcone synthase and its functions in plant resistance. Phytochem. Rev. 2011;10:397–412. doi: 10.1007/s11101-011-9211-7. PubMed DOI PMC
Ford K.L., Cassin A., Bacic A. Quantitative proteomic analysis of wheat cultivars with differing drought stress tolerance. Front. Plant Sci. 2011;2:44. doi: 10.3389/fpls.2011.00044. PubMed DOI PMC
Vincent D., Lapierre C., Pollet B., Cornic G., Negroni L., Zivy M. Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol. 2005;137:949–960. doi: 10.1104/pp.104.050815. PubMed DOI PMC
Fulda S., Mikkat S., Stegmann H., Horn R. Physiology and proteomics of drought stress acclimation in sunflower (Helianthus annuus L.) Plant Biol. 2011;13:632–642. doi: 10.1111/j.1438-8677.2010.00426.x. PubMed DOI
Zhu J., Alvarez S., Marsh E.L., LeNoble M.E., Cho I.-J., Sivaguru M., Chen S., Nguyen H.T., Wu Y., Schachtman D.P., et al. Cell wall proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol. 2007;145:1533–1548. doi: 10.1104/pp.107.107250. PubMed DOI PMC
Kong F.-J., Oyanagi A., Komatsu S. Cell wall proteome of wheat roots under flooding stress using gel-based and LC–MS/MS-based proteomics approaches. Biochim. Biophys. Acta. 2010;1804:124–136. doi: 10.1016/j.bbapap.2009.09.023. PubMed DOI
Badowiec A., Weidner S. Proteomic changes in the roots of germinating Phaseolus vulgaris seeds in response to chilling stress and post-stress recovery. J. Plant Physiol. 2014;171:389–398. doi: 10.1016/j.jplph.2013.10.020. PubMed DOI
Pang Q., Chen S., Dai S., Chen Y., Wang Y., Yan X. Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J. Proteome Res. 2010;9:2584–2599. doi: 10.1021/pr100034f. PubMed DOI
Vítámvás P., Kosová K., Prášilová P., Prášil I.T. Accumulation of WCS120 protein in wheat cultivars grown at 9 °C or 17 °C in relation to their winter survival. Plant Breed. 2010;129:611–616. doi: 10.1111/j.1439-0523.2010.01783.x. DOI
Zadražnik T., Hollung K., Egge-Jacobsen W., Meglič V., Šuštar-Vozlič J. Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.) J. Proteom. 2013;78:254–272. doi: 10.1016/j.jprot.2012.09.021. PubMed DOI
Mittler R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006;11:15–19. doi: 10.1016/j.tplants.2005.11.002. PubMed DOI
Mittler R., Blumwald E. Genetic engineering for modern agriculture: Challenges and perspectives. Annu. Rev. Plant Biol. 2010;61:443–462. doi: 10.1146/annurev-arplant-042809-112116. PubMed DOI
Li X., Cai J., Liu F., Dai T., Cao W., Jiang D. Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature. Funct. Plant Biol. 2014;41:690–703. doi: 10.1071/FP13306. PubMed DOI
Yang F., Jørgensen A.D., Li H., Søndergaard I., Finnie C., Svensson B., Jiang D., Wollenweber B., Jacobsen S. Implications of high-temperature events and water deficits on protein profiles in wheat (Triticum aestivum L. cv. Vinjett) grain. Proteomics. 2011;11:1684–1695. doi: 10.1002/pmic.201000654. PubMed DOI
Tardif G., Kane N.A., Adam H., Labrie L., Major G., Gulick P., Sarhan F., Laliberté J.F. Interaction network of proteins associated with abiotic stress response and development in wheat. Plant Mol. Biol. 2007;63:703–718. doi: 10.1007/s11103-006-9119-6. PubMed DOI
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