Proteomic Response of Hordeum vulgare cv. Tadmor and Hordeum marinum to Salinity Stress: Similarities and Differences between a Glycophyte and a Halophyte
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27536311
PubMed Central
PMC4971088
DOI
10.3389/fpls.2016.01154
Knihovny.cz E-zdroje
- Klíčová slova
- Hordeum marinum, Hordeum vulgare, glycophyte, halophyte, proteome, salinity, stress acclimation, stress damage,
- Publikační typ
- časopisecké články MeSH
Response to a high salinity treatment of 300 mM NaCl was studied in a cultivated barley Hordeum vulgare Syrian cultivar Tadmor and in a halophytic wild barley H. marinum. Differential salinity tolerance of H. marinum and H. vulgare is underlied by qualitative and quantitative differences in proteins involved in a variety of biological processes. The major aim was to identify proteins underlying differential salinity tolerance between the two barley species. Analyses of plant water content, osmotic potential and accumulation of proline and dehydrin proteins under high salinity revealed a relatively higher water saturation deficit in H. marinum than in H. vulgare while H. vulgare had lower osmotic potential corresponding with high levels of proline and dehydrins. Analysis of proteins soluble upon boiling isolated from control and salt-treated crown tissues revealed similarities as well as differences between H. marinum and H. vulgare. The similar salinity responses of both barley species lie in enhanced levels of stress-protective proteins such as defense-related proteins from late-embryogenesis abundant family, several chaperones from heat shock protein family, and others such as GrpE. However, there have also been found significant differences between H. marinum and H. vulgare salinity response indicating an active stress acclimation in H. marinum while stress damage in H. vulgare. An active acclimation to high salinity in H. marinum is underlined by enhanced levels of several stress-responsive transcription factors from basic leucine zipper and nascent polypeptide-associated complex families. In salt-treated H. marinum, enhanced levels of proteins involved in energy metabolism such as glycolysis, ATP metabolism, and photosynthesis-related proteins indicate an active acclimation to enhanced energy requirements during an establishment of novel plant homeostasis. In contrast, changes at proteome level in salt-treated H. vulgare indicate plant tissue damage as revealed by enhanced levels of proteins involved in proteasome-dependent protein degradation and proteins related to apoptosis. The results of proteomic analysis clearly indicate differential responses to high salinity and provide more profound insight into biological mechanisms underlying salinity response between two barley species with contrasting salinity tolerance.
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Ahrné E., Molzahn L., Glatter T., Schmidt A. (2013). Critical assessment of proteome-wide label-free absolute abundance estimation strategies. Proteomics 13 2567–2578. 10.1002/pmic.201300135 PubMed DOI
Ashoub A., Beckhaus T., Berberich T., Karas M., Brüggemann W. (2013). Comparative analysis of barley leaf proteome as affected by drought stress. Planta 237 771–781. 10.1007/s00425-012-1798-4 PubMed DOI
Askari H., Edqvist J., Hajheidari M., Kafi M., Salekdeh G. H. (2006). Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6 2542–2554. 10.1002/pmic.200500328 PubMed DOI
Athar H. R., Zafar Z. U., Ashraf M. (2015). Glycinebetaine improved photosynthesis in canola under salt stress: evaluation of chlorophyll fluorescence parameters as potential indicators. J. Agron. Crop Sci. 201 428–442. 10.1111/jac.12120 DOI
Barkla B. J., Vera-Estrella R., Hernandez-Coronado M., Pantoja O. (2009). Quantitative proteomics of the tonoplast reveals a role for glycolytic enzymes in salt tolerance. Plant Cell 21 4044–4058. 10.1105/tpc.109.069211 PubMed DOI PMC
Batelli G., Verslues P. E., Agius F., Qiu Q., Fujii H., Pan S. Q., et al. (2007). SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol. Cell. Biol. 27 7781–7790. 10.1128/MCB.00430-07 PubMed DOI PMC
Benchabane M., Schluüter U., Vorster J., Goulet M. C., Michaud D. (2010). Plant cystatins. Biochimie 92 1657–1666. 10.1016/j.biochi.2010.06.006 PubMed DOI
Bertoni G. (2011). CBS domain proteins regulate redox homeostasis. Plant Cell 23:3562 10.1105/tpc.111.231011 PubMed DOI PMC
Boni I. V., Isaeva D. M., Musychenko M. L., Tzareva N. V. (1991). Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res. 19 155–162. 10.1093/nar/19.1.15533 PubMed DOI PMC
Brini F., Hanin M., Lumbreras V., Irar S., Pagès M., Masmoudi K. (2007). 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. 172 20–28. 10.1016/j.plantsci.2006.07.011 DOI
Caraux G., Pinloche S. (2005). Permutmatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21 1280–1281. 10.1093/bioinformatics/bti141 PubMed DOI
Caruso G., Cavaliere C., Guarino C., Gubbiotti R., Foglia P., Laganà A. (2008). 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. 391 381–390. 10.1007/s00216-008-2008-x PubMed DOI
Chen J. H., Cheng T. L., Wang P. K., Liu W. D., Xiao J., Yang Y. Q., et al. (2012). Salinity-induced changes in protein expression in the halophytic plant Nitraria sphaerocarpa. J. Proteomics 75 5226–5243. 10.1016/j.jprot.2012.06.006 PubMed DOI
Chen S., Gollop N., Heuer B. (2009). Proteomic analysis of salt-stressed tomato (Solanum lycopersicum) seedlings: effect of genotype and exogenous application of glycinebetaine. J. Exp. Bot. 60 2005–2019. 10.1093/jxb/erp075 PubMed DOI PMC
Cheng T., Chen J., Zhang J., Shi S., Zhou Y., Lu L., et al. (2015). Physiological and proteomic analyses of leaves from the halophyte Tangut nitraria reveals diverse resposne pathways critical for high salinity tolerance. Front. Plant Sci. 6:30 10.3389/fpls.2015.00030 PubMed DOI PMC
Cheng Y., Qi Y., Zhu Q., Chen X., Wang N., Zhao X., et al. (2009). New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics 9 3100–3114. 10.1002/pmic.200800340 PubMed DOI
Choi D. W., Close T. J. (2000). A newly identified barley gene, Dhn12 encoding a YSK2 DHN, is located on chromosome 6H and has embryo-specific expression. Theor. Appl. Genet. 100 1274–1278. 10.1007/s001220051434 DOI
Choi D. W., Zhu B., Close T. J. (1999). The barley (Hordeum vulgare L.) dehydrin multigene family: sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv. Dicktoo. Theor. Appl. Genet. 98 1234–1247. 10.1007/s001220051189 DOI
Colmer T. D., Flowers T. J., Munns R. (2006). Use of wild relatives to improve salt tolerance in wheat. J. Exp. Bot. 57 1059–1078. 10.1093/jxb/erj124 PubMed DOI
Denison F. C., Paul A. L., Zupanska A. K., Ferl R. J. (2011). 14-3-3 proteins in plant physiology. Semin. Cell Dev. Biol. 22 720–727. 10.1016/j.semcdb.2011.08.006 PubMed DOI
Dooki A. D., Mayer-Posner F. J., Askari H., Zaiee A. A., Salekdeh G. H. (2006). Proteomic responses of rice young panicles to salinity. Proteomics 6 6498–6507. 10.1002/pmic.200600367 PubMed DOI
Du C. X., Fan H. F., Guo S. R., Tezuka T., Li J. (2010). Proteomic analysis of cucmber seedling roots subjected to salt stress. Phytochemistry 71 1450–1459. 10.1016/j.phytochem.2010.05.020 PubMed DOI
Durand T. C., Sergeant K., Planchon S., Carpin S., Label P., Morabito D., et al. (2010). Acute metal stress in Populus tremula x P. alba (717-1B4 genotype): leaf and cambial proteome changes induced by cadmium 2+. Proteomics 10 349–368. 10.1002/pmic.200900484 PubMed DOI
Fatehi F., Hosseinzadeh A., Alizadeh H., Brimavandi T., Struik P. C. (2012). The proteome response of salt-resistant and salt-sensitive barley genotypes to long-term salinity stress. Mol. Biol. Rep. 39 6387–6397. 10.1007/s11033-012-1460-z PubMed DOI
Finnie C., Borch J., Collinge D. B. (1999). 14-3-3 proteins: eukaryotic regulatory proteins with many functions. Plant Mol. Biol. 40 545–554. 10.1023/A:1013738603020 PubMed DOI
Flowers T. J. (2004). Improving crop salt tolerance. J. Exp. Bot. 55 307–319. 10.1093/jxb/erh003 PubMed DOI
Flowers T. J., Colmer T. D. (2015). Plant salt tolerance: adaptations in halophytes. Ann. Bot. 115 327–331. 10.1093/aob/mcu267 PubMed DOI PMC
Garthwaite A. J., von Bothmer R., Colmer T. D. (2005). Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl- into the shoots. J. Exp. Bot. 56 2365–2378. 10.1093/jxb/eri229 PubMed DOI
Geissler N., Hussin S., Koyro H. W. (2010). Elevated atmospheric CO2 concentration enhances salinity tolerance in Aster tripolium L. Planta 231 583–594. 10.1007/s00425-009-1064-6 PubMed DOI
Ghabooli M., Khatabi B., Ahmadi F. S., Sepehri M., Mirzaei M., Amirkhani A. et al. (2013). Proteomics study reveals the molecular mechanisms underlying water stress tolerance induced by Piriformospora indica in barley. J. Proteomics 94 289–301. 10.1016/j.jprot.2013.09.017 PubMed DOI
Gong Q., Li P., Ma S., Rupassara S. I., Bohnert H. J. (2005). Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J. 44 826–839. 10.1111/j.1365-313X.2005.02587.x PubMed DOI
Hlaváčková I., Vítámvás P., Šantrůèek J., Kosová K., Zelenková S., Prášil I. T., et al. (2013). Proteins involved in distinct phases of cold hardening process in frost resistant winter barley (Hordeum vulgare L.) cv. Luxor. Int. J. Mol. Sci. 44 8000–8024. 10.3390/ijms14048000 PubMed DOI PMC
Houde M., Daniel C., Lachapelle M., Allard F., Laliberté S., Sarhan F. (1995). Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J. 8 583–593. 10.1046/j.1365-313X.1995.8040583.x PubMed DOI
Hurkman W. J., Lane B. G., Tanaka C. K. (1994). Nucleotide sequence of a transcript encoding a germin-like protein that is present in salt-stressed barley (Hordeum vulgare) roots. Plant Physiol. 104 803–804. 10.1104/pp.104.2.803 PubMed DOI PMC
Islam S., Malik A. J., Islam A. K. M. R., Colmer T. D. (2007). Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. J. Exp. Bot. 58 1219-1229. 10.1093/jxb/erl293 PubMed DOI
Jang C. S., Lee H. J., Chang S. J., Seo Y. W. (2004). Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.). Plant Sci. 167 995–1001. 10.1016/j.plantsci.2004.05.019 DOI
Janská A., Aprile A., Zámečník J., Cattivelli L., Ovesná J. (2011). Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct. Integr. Genomics 11 307–325. 10.1007/s10142-011-0213-8 PubMed DOI PMC
Jiang Y., Yang B., Harris N. S., Deyholos M. K. (2007). Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J. Exp. Bot. 58 3591–3607. 10.1093/jxb/erm207 PubMed DOI
Jiménez-Bremont J. F., Becerra-Flora A., Hernández-Lucero E., Rodríguez-Kessler M., Acosta-Gallegos J. A., Ramírez-Pimentel J. G. (2006). Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine. Biol. Plant 50 763–766. 10.1007/s10535-006-0126-x DOI
Ke Y. Q., Han G. Q., He H. Q., Li J. X. (2009). Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochim. Biophys. Res. Commun. 379 133–138. 10.1016/j.bbrc.2008.12.067 PubMed DOI
Kim D. W., Rakwal R., Agrawal G. K., Jung Y. H., Shibato J., Jwa N. S., et al. (2005). A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26 4521–4539. 10.1002/elps.200500334 PubMed DOI
Komatsu S., Kamal A. H. M., Hossain Z. (2014). Wheat proteomics: proteome modulation and abiotic stress acclimation. Front. Plant Sci. 5:684 10.3389/fpls.2014.00684 PubMed DOI PMC
Kosová K., Prášil I. T., Vítámvás P. (2013a). Protein contribution to plant salinity response and tolerance acquisition. Int. J. Mol. Sci. 14 6757–6789. 10.3390/ijms14046757 PubMed DOI PMC
Kosová K., Vítámvás P., Hlaváčková I., Urban M. O., Vlasáková E., Prášil I. T. (2015). Responses of two barley cultivars differing in their salt tolerance to moderate and high salinities and subsequent recovery. Biol. Plant 59 106–114. 10.1007/s10535-014-0465-y DOI
Kosová K., Vítámvás P., Planchon S., Renaut J., Vanková R., Prášil I. T. (2013b). 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. 12 4830–4845. 10.1021/pr400600g PubMed DOI
Kosová K., Vítámvás P., Prášil I. T. (2014a). Proteomics of stress responses in wheat and barley-search for potential protein markers of stress tolerance. Front. Plant Sci. 5:711 10.3389/fpls.2014.00711 PubMed DOI PMC
Kosová K., Vítámvás P., Prášil I. T. (2014b). Wheat and barley dehydrins under cold, drought, and salinity – what can LEA-II proteins tell us about plant stress response? Front. Plant Sci. 5 343 10.3389/fpls.2014.00343 PubMed DOI PMC
Kosová K., Vítámvás P., Prášil I. T., Renaut J. (2011). Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J. Proteomics 74 1301–1322. 10.1016/j.jprot.2011.02.006 PubMed DOI
Kosová K., Vítámvás P., Prášilová P., Prášil I. T. (2013c). Accumulation of WCS120 and DHN5 proteins in differently frost-tolerant wheat and barley cultivars grown under a broad temperature scale. Biol. Plant 57 115–112. 10.1007/s10535-012-0237-5 DOI
Kosová K., Vítámvás P., Urban M. O., Prášil I. T. (2013d). Plant proteome responses to salinity stress— Comparison of glycophytes and halophytes. Funct. Plant Biol. 40 775–786. 10.1071/FP12375 PubMed DOI
Kumari A., Das P., Parida A. K., Agarwal P. K. (2015). Proteomics, metabolomics, and ionomics perspectives of salinity tolerance in halophytes. Front. Plant Sci. 6:537 10.3389/fpls.2015.00537 PubMed DOI PMC
Kwak K. J., Kim Y. O., Kang H. (2005). Characterization of transgenic Arabidopsis plants overexpressing GR-RBP4 under high salinity, dehydration, or cold stress. J. Exp. Bot. 56 3007-3016. 10.1093/jxb/eri298 PubMed DOI
Lichtenthaler H. K., Rinderle U. (1988). The role of chlorophyll fluorescence in the detection of stress conditions in plants. Crit. Rev. Anal. Chem. 19 29–85. 10.1080/15476510.1988.10401466 DOI
MacMillan C. P., Mansfield S. D., Stachurski Z. H., Evans R., Southerton S. G. (2010). Fasciclin-like arabinogalactan proteins: specialization for stem biomechanice and cell wall architecture in Arabidopsis and Eucalytpus. Plant J. 62 689–703. 10.1111/j.1365-313X.2010.04181.x PubMed DOI
Mostek A., Börner A., Badowiec A., Weidner S. (2015). Alterations in root proteome of salt-sensitive and tolerant barley lines under salt stress conditions. J. Plant Physiol. 174 166–176. 10.1016/j.jplph.2014.08.0200176-1617 PubMed DOI
Munns R. (2002). Comparative physiology of salt and water stress. Plant Cell Environ. 25 239–250. 10.1046/j.0016-8025.2001.00808.x PubMed DOI
Munns R., Tester M. (2008). Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59 651–681. 10.1146/annurev.arplant.59.032607.092911 PubMed DOI
Pang Q., Chen S., Dai S., Chen Y., Wang Y., Yan X. (2010). Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J. Proteome Res. 9 2584–2599. 10.1021/pr100034f PubMed DOI
Park S. Y., Fung P., Nishimura N., Jensen D. R., Fujii H., Zhao Y., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324 1068–1071. 10.1126/science.1173041 PubMed DOI PMC
Peng Z., Wang M., Li F., Lv H., Li C., Xia G. (2009). A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol. Cell. Proteomics 8 2676–2686. 10.1074/mcp.M900052-MCP200 PubMed DOI PMC
Prášil I. T., Prášilová P., Pánková K. (2005). The relationship between vernalization requirement and frost tolerance in substitution lines of wheat. Biol. Plant 49 195–200. 10.1007/s10535-005-5200-2 DOI
Puranik S., Sahu P. P., Srivatsava P. S., Prasad M. (2012). NAC proteins: regulation and role in stress toelrance. Trends Plant Sci. 17 369–381. 10.1016/j.tplants.2012.02.004 PubMed DOI
Quesada V., Dean C., Simpson G. G. (2005). Regulated RNA processing in the control of Arabidopsis flowering. Int. J. Dev. Biol. 49 773-780. 10.1387/ijdb.051995vq PubMed DOI
Rasoulnia A., Bihamta M. R., Peyghambari S. A., Alizadeh H., Rahnama A. (2011). Proteomic response of barley leaves to salinity. Mol. Biol. Rep. 38 5055–5063. 10.1007/s11033-010-0651-8 PubMed DOI
Rinalducci S., Egidi K. G., Mahfoozi S., Godehkahriz S. J., Zolla L. (2011). The influence of temperature on plant development in a vernalization-requiring winter wheat: a 2-DE based proteomic investigation. J. Proteomics 74 643–659. 10.1016/j.jprot.2011.02.005 PubMed DOI
Rizza F., Pagani D., Gut M., Prášil I. T., Lago C., Tondelli A., et al. (2011). Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci. 51 2759–2779. 10.2135/cropsci2011.01.0005 DOI
Rodriguez E. M., Svensson J. T., Malatrasi M., Choi D. W., Close T. J. (2005). Barley Dhn13 encodes a KS-type dehydrin with constitutive and stress responsive expression. Theor. Appl. Genet. 110 852–858. 10.1007/s00122-004-1877-4 PubMed DOI
Schauber C., Chen L., Tongaonkar P., Vega I., Lambertson D., Potts W., et al. (1998). Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391 715–718. 10.1038/35661 PubMed DOI
Sengupta S., Majumder A. L. (2009). Insight into the salt tolerance factors of a wild halophytic rice, Porteresia. coarctata: a physiological and proteomic approach. Planta 229 911–929. 10.1007/s00425-008-0878-y PubMed DOI
Singh A. K., Kumar R., Pareek A., Sopory S. K., Singla-Pareek S. L. (2012). Overexpression of rice CBS domain containing protein improves salinity, oxidative, and heavy metal tolerance in transgenic tobacco. Mol. Biotechnol. 52 205–216. 10.1007/s12033-011-9487-2 PubMed DOI
Slavík B. (1963). Relationship between the osmotic potential of cell sap and the water saturation deficit during the wilting of leaf tissue. Biol. Plant 5 258–264. 10.1007/BF02930904 DOI
Sobhanian H., Motamed N., Jazii F. R., Nakamura T., Komatsu S. (2010). Saltstress induced differential proteome and metabolome response in the shoots of Aeluropus lagopoides (Poaceae), a halophyte C4 plant. J. Proteome Res. 9 2882–2897. 10.1021/pr900974k PubMed DOI
Streitner C., Danisman S., Wehrle F., Schoöning J. C., Alfano J. R., Staiger D. (2008). The small glycine-rich RNA binding protein AtGRP7 promotes floral transition in Arabidopsis thaliana. Plant J. 56 239–250. 10.1111/j.1365-313X.2008.03591.x PubMed DOI
Suzuki N., Koussevitzky S., Mittler R., Miller G. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35 259–270. 10.1111/j.1365-3040.2011.02336.x PubMed DOI
Tada Y., Kashimura T. (2009). Proteomic analysis of salt-responsive proteinsin the mangrove plant, Bruguiera gymnorhiza. Plant Cell Physiol. 50 439–446. 10.1093/pcp/pcp002 PubMed DOI
Taji T., Seki M., Satou M., Sakurai T., Kobayashi M., Ishiyama K., et al. (2004). Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol. 135 1697–1709. 10.1104/pp.104.039909 PubMed DOI PMC
Tamás L., Simonovicová M., Huttová J., Mistrík I. (2004). Elevated oxalate oxidase activity is correlated with Al-induced plasma membrane injury and root growth inhibition in young barley roots. Acta Physiol. Plant 26 85-93. 10.1007/s11738-004-0048-1 DOI
Thompson J. E., Hopkins M. T., Taylor C., Wang T. W. (2004). Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci. 9 174–179. 10.1016/j.tplants.2004.02.008 PubMed DOI
Tommasini L., Svensson J. T., Rodriguez E. M., Wahid A., Malatrasi M., Kato K., et al. (2008). Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct. Integr. Genomics 8 387–405. 10.1007/s10142-008-0081-z PubMed DOI
Udawat P., Jha R. K., Sinha D., Mishra A., Jha B. (2016). Overexpression of a cytosolic abiotic stress responsive universal stress protein (SbUSP) mitigates salt and osmotic stress in transgenic tobacco plants. Front. Plant Sci. 7:518 10.3389/flps.2016.00518 PubMed DOI PMC
Valentovicová K., Halusková L., Huttová J., Mistrík I., Tamás L. (2009). Effect of heavy metals and temperature on the oxalate oxidase activity and lignification of metaxylem vessels in barley roots. Environ. Exp. Bot. 66 457–462. 10.1016/j.envexpbot.2009.03.006 DOI
Vincent D., Ergül A., Bohlman M. C., Tattersall E. A. R., Tillett R. L., Wheatley M. D., et al. (2007). 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. 58 1873–1892. 10.1093/jxb/erm012 PubMed DOI
Vítámvás P., Prášil I. T., Kosová K., Planchon S., Renaut J. (2012). Analysis of proteome and frost tolerance in chromosome 5A and 5B reciprocal substitution lines between two winter wheats during long-term cold acclimation. Proteomics 12 68–85. 10.1002/pmic.201000779 PubMed DOI
Vítámvás P., Urban M. O., Škodáček Z., Kosová K., Pitelková I., Vítámvás J., et al. (2015). Quantitative analysis of proteome extracted from barley crowns grown under different drought conditions. Front. Plant Sci. 6:479 10.3389/fpls.2015.00479 PubMed DOI PMC
Wang C., Zhang D. W., Wang Y. C., Zheng L., Yang C. P. (2012). A glycine-rich RNA-binding protein can mediate physiological responses in transgenic plants under salt stress. Mol. Biol. Rep. 39 1047–1053. 10.1007/s11033-011-0830-2 PubMed DOI
Wang J., Meng Y., Li B., Ma X., Lai Y., Si E., et al. (2015). Physiological and proteomic analyses of salt stress response in the halophyte Halogeton glomeratus. Plant Cell Environ. 38 655–669. 10.1111/pce.12428 PubMed DOI PMC
Wang L., Liu X., Liang M., Tan F., Liang W., Chen Y., et al. (2014). Proteomic analysis of salt-responsive proteins in the leaves of mangrove Kandelia candel during short-term stress. PLoS ONE 9:e83141 10.1371/journal.pone.0083141 PubMed DOI PMC
Wang M. C., Peng Z. Y., Li C. L., Li F., Liu C., Xia G. M. (2008). Proteomic analysis on a high salt tolerance introgression strain of Triticum aestivum/Thinopyrum ponticum. Proteomics 8 1470–1489. 10.1002/pmic.200700569 PubMed DOI
Witzel K., Weidner A., Surabhi G. K., Börner A., Mock H. P. (2009). Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J. Exp. Bot. 60 3545–3557. 10.1093/jxb/erp198 PubMed DOI PMC
Xu C., Sibicky T., Huang B. (2010). Protein profile analysis of salt-responsive proteins in leaves and roots in two cultivars of creeping bentgrass differing in salinity tolerance. Plant Cell Rep. 29 595–615. 10.1007/s00299-010-0847-3 PubMed DOI
Yamaguchi-Shinozaki K., Shinozaki K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57 781–803. 10.1146/annurev.arplant.57.032905.105444 PubMed DOI
Yan S., Tang Z., Su W., Sun W. (2005). Proteomic analysis of salt stress responsiveproteins in rice root. Proteomics 5 235–244. 10.1002/pmic.200400853 PubMed DOI
Yu J., Chen S., Zhao Q., Wang T., Yang C., Diaz C., et al. (2011). Physiological and proteomic analysis of salinity tolerance in Puccinellia tenuiflora. J. Proteome Res. 10 3852–3870. 10.1021/pr101102p PubMed DOI
Zhang M., Lv D., Ge P., Bian Y., Chen G., Zhu G., et al. (2014). Phosphoproteome analysis reveals new drought response and defense mechanisms of seedling leaves in bread wheat (Triticum aestivum L.). J. Proteomics 109 290–308. 10.1016/j.jprot.2014.07.010 PubMed DOI
Zhou F., Zhang Z., Gregersen P., Mikkelsen J., de Neergaard E., Collinge D., et al. (1998). Molecular characterization of oxalate oxidase involved in the response of barley to the powdery mildew fungus. Plant Physiol. 117 33–41. 10.1104/pp.117.1.33 PubMed DOI PMC
Zhu J. K. (2001). Plant salt tolerance. Trends Plant Sci. 6 66–71. 10.1016/S1360-1385(00)01838-0 PubMed DOI
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