Global Scale Transcriptional Profiling of Two Contrasting Barley Genotypes Exposed to Moderate Drought Conditions: Contribution of Leaves and Crowns to Water Shortage Coping Strategies
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28083001
PubMed Central
PMC5187378
DOI
10.3389/fpls.2016.01958
Knihovny.cz E-zdroje
- Klíčová slova
- Amulet, Tadmor, barley, crown, drought, leaf, microarray,
- Publikační typ
- časopisecké články MeSH
Drought is a serious threat for sustainable agriculture. Barley represents a species well adapted to environmental stresses including drought. To elucidate the adaptive mechanism of barley on transcriptional level we evaluated transcriptomic changes of two contrasting barley cultivars upon drought using the microarray technique on the level of leaves and crowns. Using bioinformatic tools, differentially expressed genes in treated vs. non-treated plants were identified. Both genotypes revealed tissue dehydration under drought conditions as shown at water saturation deficit and osmotic potential data; however, dehydration was more severe in Amulet than in drought-resistant Tadmor under the same ambient conditions. Performed analysis showed that Amulet enhanced expression of genes related to active plant growth and development, while Tadmor regarding the stimulated genes revealed conservative, water saving strategy. Common reactions of both genotypes and tissues included an induction of genes encoding several stress-responsive signaling proteins, transcription factors as well as effector genes encoding proteins directly involved in stress acclimation. In leaf, tolerant cultivar effectively stimulated mainly the expression of genes encoding proteins and enzymes involved in protein folding, sulfur metabolism, ROS detoxification or lipid biosynthesis and transport. The crown specific reaction of tolerant cultivar was an enhanced expression of genes encoding proteins and enzymes involved in cell wall lignification, ABRE-dependent abscisic acid (ABA) signaling, nucleosome remodeling, along with genes for numerous jasmonate induced proteins.
Division of Crop Genetics and Breeding Crop Research Institute Prague Czechia
Faculty of Food and Biochemical Technology University of Chemistry and Technology Prague Czechia
Zobrazit více v PubMed
Al-Abdallat A. M., Al-Debei H. S., Ayad J. Y., Hasan S. (2014). Over-Expression of SlSHN1 gene improves drought tolerance by increasing cuticular wax accumulation in tomato. Int. J. Mol. Sci. 15 19499–19515. 10.3390/ijms151119499 PubMed DOI PMC
Araus J. L., Slafer G. A., Royo C., Serret M. D. (2008). Breeding for yield potential and stress adaptation in cereals. Crit. Rev. Plant Sci. 27 377–412. 10.1080/07352680802467736 DOI
Arora R., Agarwal P., Ray S., Singh A. K., Singh V. P., Tyagi A. K., et al. (2007). MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242 10.1186/1471-2164-8-242 PubMed DOI PMC
Asch F. (2000). Laboratory Manual on Determination of Abscisic Acid by Indirect Enzyme Linked Immuno Sorbent Assay (ELISA). Frederiksberg: Royal Veterinary and Agricultural University.
Atienza S. G., Faccioli P., Perrotta G., Dalfino G., Zschiesche W., Humbeck K., et al. (2004). Large scale analysis of transcripts abundance in barley subjected to several single and combined abiotic stress conditions. Plant Sci. 167 1359–1365. 10.1016/j.plantsci.2004.07.006 DOI
Augustine S. M., Narayan J. A., Syamaladevi D. P., Appunu C., Chakravarthi M., Ravichandran V., et al. (2015). Erianthus arundinaceus HSP70 (EaHSP70) overexpression increases drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Sci. 232 23–34. 10.1016/j.plantsci.2014.12.012 PubMed DOI
Aziz A., Larher F. (1998). Osmotic stress induced changes in lipid composition and peroxidation in leaf discs of Brassica napus L. J. Plant Physiol. 153 754–762. 10.1016/S0176-1617(98)80231-9 DOI
Beddington J., Asaduzzaman M., Fernandez A., Clark M., Guillou M., Jahn M., et al. (2011). Achieving Food Security in the Face of Climate Change: Summary for Policy Makers From the Commission on Sustainable Agriculture and Climate Change. Copenhagen: CGIAR Research Program on Climate Change.
Blum A., Ebercon A. (1981). Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci. 21 43–47. 10.2135/cropsci1981.0011183X002100010013x DOI
Bohlmann H., Clausen S., Behnke S., Giese H., Hiller C., Reimann-Philipp U., et al. (1988). Leaf-specific thionins of barley–a novel class of cell wall proteins toxic to plant-pathogenic fungi and possibly involved in the defence mechanism of plants. EMBO J. 7 1559. PubMed PMC
Boyer J. S. (1982). Plant productivity and environment. Science 218 443–448. 10.1126/science.218.4571.443 PubMed DOI
Bruinsma J. (2009). The resource outlook to 2050. by how much do land, water and crop yields need to increase by 2050? Paper Presented at the FAO Expert Meeting How to Feed the World in 2050? Rome: 1–33.
Carmona M. J., Molina A., Fernández J. A., López-Fando J. J., García-Olmedo F. (1993). Expression of the E-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens. Plant J. 3 457–462. 10.1111/j.1365-313X.1993.tb00165.x PubMed DOI
Cattivelli L., Rizza F., Badeck F. W., Mazzucotelli E., Mastrangelo A. M., Francia E., et al. (2008). Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop. Res. 105 1–14. 10.1016/j.fcr.2007.07.004 DOI
Ceccarelli S. (1994). “Specific adaptation and breeding for marginal conditions,” in Breeding Fodder Crops for Marginal Conditions eds Rognli O. A., Solberg E. T., Schjelderup I. (Dordrecht: Springer; ) 101–127. 10.1007/978-94-011-0966-6_15 DOI
Chalker-Scott L. (1999). Environmental significance of anthocyanins in plant stress responses. Photochem. Photobiol. 70 1–9. 10.1111/j.1751-1097.1999.tb01944.x DOI
Chan K. X., Wirtz M., Phua S. Y., Estavillo G. M., Pogson B. J. (2013). Balancing metabolites in drought: the sulfur assimilation conundrum. Trends Plant Sci. 18 18–29. 10.1016/j.tplants.2012.07.005 PubMed DOI
Chaudhry B., Müller-Uri F., Cameron-Mills V., Gough S., Simpson D., Skriver K., et al. (1994). The barley 60 kDa jasmonate-induced protein (JIP60) is a novel ribosome-inactivating protein. Plant J. 6 815–824. 10.1046/j.1365-313X.1994.6060815.x PubMed DOI
Chaves M. M., Flexas J., Pinheiro C. (2009). Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 103 551–560. 10.1093/aob/mcn125 PubMed DOI PMC
Chen G., Komatsuda T., Ma J. F., Li C., Yamaji N., Nevo E. (2011). A functional cutin matrix is required for plant protection against water loss. Plant Signal. Behav. 6 1297–1299. 10.4161/psb.6.9.17507 PubMed DOI PMC
Chen H. (2013). VennDiagram: Generate High-Resolution Venn and Euler plots. R package version 1.6.5. Available at: http://CRAN.R-project.org/package=VennDiagram
Chen K. M., Holmström M., Raksajit W., Suorsa M., Piippo M., Aro E. M. (2010). Small chloroplast-targeted DnaJ proteins are involved in optimization of photosynthetic reactions in Arabidopsis thaliana. BMC Plant Biol. 10:43 10.1186/1471-2229-10-43 PubMed DOI PMC
Chi W. C., Chen Y. A., Hsiung Y. C., Fu S. F., Chou C. H., Trinh N. N., et al. (2013). Autotoxicity mechanism of Oryza sativa: transcriptome response in rice roots exposed to ferulic acid. BMC Genomics 14:351 10.1186/1471-2164-14-351 PubMed DOI PMC
Cho E. K., Choi Y. J. (2009). A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol. Lett. 31 597–606. 10.1007/s10529-008-9880-5 PubMed DOI
Cho E. K., Hong C. B. (2006). Over-expression of tobacco NtHSP70-1 contributes to drought-stress tolerance in plants. Plant Cell Rep. 25 349–358. 10.1007/s00299-005-0093-2 PubMed DOI
Close T. J., Wanamaker S. I., Caldo R. A., Turner S. M., Ashlock D. A., Dickerson J. A., et al. (2004). A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiol. 134 960–968. 10.1104/pp.103.034462 PubMed DOI PMC
Cominelli E., Galbiati M., Vavasseur A., Conti L., Sala T., Vuylsteke M., et al. (2005). A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr. Biol. 15 1196–1200. 10.1016/j.cub.2005.05.048 PubMed DOI
Cruz R. T., Jordan W. R., Drew M. C. (1992). Structural changes and associated reduction of hydraulic conductance in roots of Sorghum bicolor L. following exposure to water deficit. Plant Physiol. 99 203–212. 10.1104/pp.99.1.203 PubMed DOI PMC
Cyr D. M., Langer T., Douglas M. G. (1994). DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends Biochems. Sci. 19 176–181. 10.1016/0968-0004(94)90281-X PubMed DOI
Dai X., Xu Y., Ma Q., Xu W., Wang T., Xue Y., et al. (2007). Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol. 143 1739–1751. 10.1104/pp.106.094532 PubMed DOI PMC
Deeba F., Pandey A. K., Ranjan S., Mishra A., Singh R., Sharma Y. K., et al. (2012). Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. Plant Physiol. Biochem. 53 6–18. 10.1016/j.plaphy.2012.01.002 PubMed DOI
del Pozo J. C., Allona I., Rubio V., Leyva A., De La Peña A., Aragoncillo C., et al. (1999). A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions. Plant J. 19 579–589. 10.1046/j.1365-313X.1999.00562.x PubMed DOI
DeLaat D. M., Colombo C. A., Chiorato A. F., Carbonell S. A. M. (2014). Induction of ferritin synthesis by water deficit and iron excess in common bean (Phaseolus vulgaris L.). Mol. Biol. Rep. 41 1427–1435. 10.1007/s11033-013-2987-3 PubMed DOI
Ding Y., Liu N., Virlouvet L., Riethoven J. J., Fromm M., Avramova Z. (2013). Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 13:1 10.1186/1471-2229-13-229 PubMed DOI PMC
Ding Z., Li S., An X., Liu X., Qin H., Wang D. (2009). Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J. Genet. Genomics 36 17–29. 10.1016/S1673-8527(09)60003-5 PubMed DOI
Epple P., Apel K., Bohlmann H. (1997). Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum. The Plan cell 9 509–520. 10.1105/tpc.9.4.509 PubMed DOI PMC
Faostat. (2016). Available at. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor. (accessed January 12, 2015)
Farooq M., Wahid A., Lee D. J. (2009). Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol. Plant. 31 937–945. 10.1007/s11738-009-0307-2 DOI
Field C. B. (ed.) (2012). Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation: Special Report of The Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press; 10.1017/CBO9781139177245 PubMed DOI
Fowler S., Thomashow M. F. (2002). Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14 1675–1690. 10.1105/tpc.003483 PubMed DOI PMC
Fujita Y., Fujita M., Satoh R., Maruyama K., Parvez M. M., Seki M., et al. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. The Plan cell 17 3470–3488. 10.1105/tpc.105.035659 PubMed DOI PMC
Gao S., Guo W., Feng W., Liu L., Song X., Chen J., et al. (2015). LTP3 contributes to disease susceptibility in Arabidopsis by enhancing abscisic acid (ABA) biosynthesis. Mol. Plant Pathol. 17 412–426. 10.1111/mpp.12290 PubMed DOI PMC
Gautier L., Cope L., Bolstad B. M., Irizarry R. A. (2004). Affy–analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20 307–315. 10.1093/bioinformatics/btg405 PubMed DOI
Godfray H. C. J., Beddington J. R., Crute I. R., Haddad L., Lawrence D., Muir J. F., et al. (2010). Food security: the challenge of feeding 9 billion people. Science 327 812–818. 10.1126/science.1185383 PubMed DOI
Goyal K., Walton L. J., Tunnacliffe A. (2005). LEA proteins prevent protein aggregation due to water stress. Biochem. J. 388 151–157. 10.1042/BJ20041931 PubMed DOI PMC
Gregory P. J., George T. S. (2011). Feeding nine billion: the challenge to sustainable crop production. J. Exp. Bot. 62 5233–5239. 10.1093/jxb/err232 PubMed DOI
Grigorova B., Vaseva I., Demirevska K., Feller U. (2011a). Combined drought and heat stress in wheat: changes in some heat shock proteins. Biol. Plant. 55 105–111. 10.1007/s10535-011-0014-x DOI
Grigorova B., Vaseva I. I., Demirevska K., Feller U. (2011b). Expression of selected heat shock proteins after individually applied and combined drought and heat stress. Acta Physiol. Plant. 33 2041–2049. 10.1007/s11738-011-0733-9 DOI
Gu D., Liu X., Wang M., Zheng J., Hou W., Wang G., et al. (2008). Overexpression of ZmOPR1 in Arabidopsis enhanced the tolerance to osmotic and salt stress during seed germination. Plant Sci. 174 124–130. 10.1016/j.plantsci.2007.09.010 DOI
Guo D., Chen F., Wheeler J., Winder J., Selman S., Peterson M., et al. (2001). Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res. 10 457–464. 10.1023/A:1012278106147 PubMed DOI
Guo P., Baum M., Grando S., Ceccarelli S., Bai G., Li R., et al. (2009). Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J. Exp. Bot. 60 3531–3544. 10.1093/jxb/erp194 PubMed DOI PMC
Guo P., Baum M., Li R., Grando S., Varshney R. K., Graner A., et al. (2007). Transcriptional analysis of barley genes in response to drought stress at the reproductive growth stage using Affymetrix Barley 1 genechip. J. Guangzhou University (Nat. Sci. Ed.) 6 32–36.
Hause B., Demus U., Teichmann C., Parthier B., Wasternack C. (1996). Developmental and tissue-specific expression of JIP-23, a jasmonate-inducible protein of barley. Plant Cell Physiol. 37 641–649. 10.1093/oxfordjournals.pcp.a028993 PubMed DOI
Havaux M., Tardy F. (1999). Loss of chlorophyll with limited reduction of photosynthesis as an adaptive response of Syrian barley landraces to high-light and heat stress. Funct. Plant Biol. 26 569–578. 10.1071/PP99046 DOI
Hu Y., Li W. C., Xu Y. Q., Li G. J., Liao Y., Fu F. L. (2009). Differential expression of candidate genes for lignin biosynthesis under drought stress in maize leaves. J. Appl. Genet. 50 213–223. 10.1007/BF03195675 PubMed DOI
Hura T., Grzesiak S., Hura K., Thiemt E., Tokarz K., Wêdzony M. (2007). Physiological and biochemical tools useful in drought-tolerance detection in genotypes of winter triticale: accumulation of ferulic acid correlates with drought tolerance. Ann. Bot. London 100 767–775. 10.1093/aob/mcm162 PubMed DOI PMC
Hura T., Hura K., Grzesiak S. (2008). Contents of total phenolics and ferulic acid, and PAL activity during water potential changes in leaves of maize single-cross hybrids of different drought tolerance. J. Agron. Crop Sci. 194 104–112. 10.1111/j.1439-037X.2008.00297.x DOI
Hura T., Hura K., Grzesiak S. (2009). Leaf dehydration induces different content of phenolics and ferulic acid in drought-resistant and-sensitive genotypes of spring triticale. Z. Naturforsch. C 64 85 10.1515/znc-2009-1-215 PubMed DOI
Irizarry R. A., Hobbs B., Collin F., Beazer-Barclay Y. D., Antonellis K. J., Scherf U., et al. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 249–264. 10.1093/biostatistics/4.2.249 PubMed DOI
Janská A., Aprile A., Cattivelli L., Zámečník J., de Bellis L., Ovesná J. (2014). The up-regulation of elongation factors in the barley leaf and the down-regulation of nucleosome assembly genes in the crown are both associated with the expression of frost tolerance. Funct. Integr. Genomics 14 493–506. 10.1007/s10142-014-0377-0 PubMed 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 T., Fountain J., Davis G., Kemerait R., Scully B., Lee R. D., et al. (2012). Root morphology and gene expression analysis in response to drought stress in maize (Zea mays). Plant Mol. Biol. Rep. 30 360–369. 10.1007/s11105-011-0347-9 DOI
Kar M., Mishra D. (1976). Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol. 57 315–319. 10.1104/pp.57.2.315 PubMed DOI PMC
Kawasaki S., Borchert C., Deyholos M., Wang H., Brazille S., Kawai K., et al. (2001). Gene expression profiles during the initial phase of salt stress in rice. Plant cell 13 889–905. 10.1105/tpc.13.4.889 PubMed DOI PMC
Kawaura K., Mochida K., Yamazaki Y., Ogihara Y. (2006). Transcriptome analysis of salinity stress responses in common wheat using a 22k oligo-DNA microarray. Funct. Integr. Genomics 6 132–142. 10.1007/s10142-005-0010-3 PubMed DOI
Kim S., Kang J. Y., Cho D. I., Park J. H., Kim S. Y. (2004). ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 40 75–87. 10.1111/j.1365-313X.2004.02192.x PubMed DOI
Kosová K., Prášil I. T., Prášilová P., Vítámvás P., Chrpová J. (2010). The development of frost tolerance and DHN5 protein accumulation in barley (Hordeum vulgare) doubled haploid lines derived from Atlas 68 × Igri cross during cold acclimation. J. Plant Physiol. 167 343–350. 10.1016/j.jplph.2009.09.020 PubMed DOI
Laemmli U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680–685. 10.1038/227680a0 PubMed DOI
Lagrimini L. M., Bradford S., Rothstein S. (1990). Peroxidase-induced wilting in transgenic tobacco plants. Plant Cell 2 7–18. 10.2307/3869046 PubMed DOI PMC
Li W. Y. F., Shao G., Lam H. M. (2008). Ectopic expression of GmPAP3 alleviates oxidative damage caused by salinity and osmotic stresses. New Phytol. 178 80–91. 10.1111/j.1469-8137.2007.02356.x PubMed DOI
Li X., Zhuo J., Jing Y., Liu X., Wang X. (2011). Expression of a GALACTINOL SYNTHASE gene is positively associated with desiccation tolerance of Brassica napus seeds during development. J. Plant Physiol. 168 1761–1770. 10.1016/j.jplph.2011.04.006 PubMed DOI
Liu J. J. J., Krenz D. C., Galvez A. F., de Lumen B. O. (1998). Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation. Plant Sci. 134 11–20. 10.1016/S0168-9452(98)00042-9 DOI
Lucas A. (2014). amap: Another Multidimensional Analysis Package. R package version 0.8-12. Available at: http://CRAN.R-project.org/package=amap
Martin C., Paz-Ares J. (1997). MYB transcription factors in plants. Trends Genet. 13 67–73. 10.1016/S0168-9525(96)10049-4 PubMed DOI
Molina A., Goy P. A., Fraile A., Sánchez-Monge R., García-Olmedo F. (1993). Inhibition of bacterial and fungal plant pathogens by thionins of types I and II. Plant Sci. 92 169–177. 10.1016/0168-9452(93)90203-C DOI
Muchero W., Roberts P. A., Diop N. N., Drabo I., Cisse N., Close T. J., et al. (2013). Genetic architecture of delayed senescence, biomass, and grain yield under drought stress in cowpea. PLoS ONE 8:e70041 10.1371/journal.pone.0070041 PubMed DOI PMC
Mukhopadhyay A., Vij S., Tyagi A. K. (2004). Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc. Natl. Acad. Sci. U.S.A. 101 6309–6314. 10.1073/pnas.0401572101 PubMed DOI PMC
Muramoto N., Tanaka T., Shimamura T., Mitsukawa N., Hori E., Koda K., et al. (2012). Transgenic sweet potato expressing thionin from barley gives resistance to black rot disease caused by Ceratocystis fimbriata in leaves and storage roots. Plant Cell Rep. 31 987–997. 10.1007/s00299-011-1217-5 PubMed DOI
Nakabayashi R., Yonekura-Sakakibara K., Urano K., Suzuki M., Yamada Y., Nishizawa T., et al. (2014). Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77 367–379. 10.1111/tpj.12388 PubMed DOI PMC
Nakashima K., Takasaki H., Mizoi J., Shinozaki K., Yamaguchi-Shinozaki K. (2012). NAC transcription factors in plant abiotic stress responses. BBA-Gene Regul. Mech. 1819 97–103. 10.1016/j.bbagrm.2011.10.005 PubMed DOI
Nakashima K., Tran L. S. P., Van Nguyen D., Fujita M., Maruyama K., Todaka D., et al. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51 617–630. 10.1111/j.1365-313X.2007.03168.x PubMed DOI
Nevo E. (1992). “Origin, evolution, population genetics and resources for breeding of wild barley, Hordeum spontaneum, in the Fertile Crescent,” in Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology ed. Shewry P. (Wallingford: CAB Int; ) 19–43.
Ouimet P. M., Kapoor M. (1998). Analysis of complex formation between Hsp80 and Hsp70, cytosolic molecular chaperones of Neurospora crassa, by enzyme-linked immunosorbent assays (ELISA). Biochem. Cell Biol. 76 97–106. 10.1139/098-010 PubMed DOI
Ozturk Z. N., Talamé V., Deyholos M., Michalowski C. B., Galbraith D. W., Gozukirmizi N., et al. (2002). Monitoring large-scale changes in transcript abundance in drought-and salt-stressed barley. Plant Mol. Biol. 48 551–573. 10.1023/A:1014875215580 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
Peleg Z., Apse M. P., Blumwald E. (2011). Engineering salinity and water-stress tolerance in crop plants: getting closer to the field. Adv. Bot. Res. 57 405–443. 10.1016/B978-0-12-387692-8.00012-6 DOI
Pellegrineschi A., Noguera L. M., Skovmand B., Brito R. M., Velazquez L., Salgado M. M., et al. (2002). Identification of highly transformable wheat genotypes for mass production of fertile transgenic plants. Genome 45 421–430. 10.1139/g01-154 PubMed DOI
Pellegrineschi A., Reynolds M., Pacheco M., Brito R. M., Almeraya R., Yamaguchi-Shinozaki K., et al. (2004). Stress-induced expression in wheat of the Arabidopsis thaliana DREB1A gene delays water stress symptoms under greenhouse conditions. Genome 47 493–500. 10.1139/g03-140 PubMed DOI
Pollard M., Beisson F., Li Y., Ohlrogge J. B. (2008). Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13 236–246. 10.1016/j.tplants.2008.03.003 PubMed DOI
Qin Y., Wang M., Tian Y., He W., Han L., Xia G. (2012). Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Mol. Biol. Rep. 39 7183–7192. 10.1007/s11033-012-1550-y PubMed DOI
Quartacci M. F., Pinzino C., Sgherri C. L., Navari-Izzo F. (1995). Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought. Plant Physiol. 108 191–197. 10.1104/pp.108.1.191 PubMed DOI PMC
R Core Team (2015). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
Ristic Z., Yang G., Martin B., Fullerton S. (1998). Evidence of association between specific heat-shock protein (s) and the drought and heat tolerance phenotype in maize. J. Plant Physiol. 153 497–505. 10.1016/S0176-1617(98)80180-6 DOI
Rivero R. M., Kojima M., Gepstein A., Sakakibara H., Mittler R., Gepstein S., et al. (2007). Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. U.S.A. 104 19631–19636. 10.1073/pnas.0709453104 PubMed DOI PMC
Rodrigues A., Adamo M., Crozet P., Margalha L., Confraria A., Martinho C., et al. (2013). ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25 3871–3884. 10.1105/tpc.113.114066 PubMed DOI PMC
Rosado A., Schapire A. L., Bressan R. A., Harfouche A. L., Hasegawa P. M., Valpuesta V., et al. (2006). The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol. 142 1113–1126. 10.1104/pp.106.085191 PubMed DOI PMC
Saeedipour S., Moradi F. (2012). Stress-induced changes in the free amino acid composition of two wheat cultivars with difference in drought resistance. Afr. J. Biotechnol. 11 9559.
Santino A., Taurino M., De Domenico S., Bonsegna S., Poltronieri P., Pastor V., et al. (2013). Jasmonate signaling in plant development and defense response to multiple (a) biotic stresses. Plant Cell Rep. 32 1085–1098. 10.1007/s00299-013-1441-2 PubMed DOI
Sarkar N. K., Kundnani P., Grover A. (2013). Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18 427–437. 10.1007/s12192-012-0395-6 PubMed DOI PMC
Seki M., Narusaka M., Abe H., Kasuga M., Yamaguchi-Shinozaki K., Carninci P., et al. (2001). Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13 61–72. 10.1105/tpc.13.1.61 PubMed DOI PMC
Sembdner G. A. P. B., Parthier B. (1993). The biochemistry and the physiological and molecular actions of jasmonates. Annu. Rev. Plant Biol. 44 569–589. 10.1146/annurev.pp.44.060193.003033 DOI
Seo P. J., Park C. M. (2011). Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signal. Behav. 6 1043–1045. 10.4161/psb.6.7.15606 PubMed DOI PMC
Slavík B. (1974). Methods of Studying Plant Water Relations. Prague: Academia, Publishing House of the Czechoslovak Academy of Sciences; 449.
Smyth G. K. (2005). “Limma: linear models for microarray data,” in Bioinformatics and Computational Biology Solutions Using R and Bioconductor eds Gentleman R., Carey V. J., Huber W., Irizarry R. A., Dudoit S. (New York, NY: Springer; ) 397–420.
Song Y., Masison D. C. (2005). Independent regulation of Hsp70 and Hsp90 chaperones by Hsp70/Hsp90-organizing protein Sti1 (Hop1). J. Biol. Chem. 280 34178–34185. 10.1074/jbc.M505420200 PubMed DOI PMC
Sun Z., Qi X., Wang Z., Li P., Wu C., Zhang H., et al. (2013). Overexpression of TsGOLS2, a galactinol synthase, in Arabidopsis thaliana enhances tolerance to high salinity and osmotic stresses. Plant Physiol. Biochem. 69 82–89. 10.1016/j.plaphy.2013.04.009 PubMed DOI
Szabados L., Savoure A. (2010). Proline: a multifunctional amino acid. Trends Plant Sci. 15 89–97. 10.1016/j.tplants.2009.11.009 PubMed DOI
Taji T., Ohsumi C., Iuchi S., Seki M., Kasuga M., Kobayashi M., et al. (2002). Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29 417–426. 10.1046/j.0960-7412.2001.01227.x PubMed DOI
Takatsuji H. (1998). Zinc-finger transcription factors in plants. Cell. Mol. Life Sci. 54 582–596. 10.1007/s000180050186 PubMed DOI PMC
Talamè V., Ozturk N. Z., Bohnert H. J., Tuberosa R. (2007). Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J. Exp. Bot. 58 229–240. 10.1093/jxb/erl163 PubMed DOI
Tardy F., Créach A., Havaux M. (1998). Photosynthetic pigment concentration, organization and interconversions in a pale green Syrian landrace of barley (Hordeum vulgare L., Tadmor) adapted to harsh climatic conditions. Plant Cell Environ. 21 479–489. 10.1046/j.1365-3040.1998.00293.x DOI
Thimm O., Essigmann B., Kloska S., Altmann T., Buckhout T. J. (2001). Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol. 127 1030–1043. 10.1104/pp.010191 PubMed DOI PMC
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
Toumi I., Gargouri M., Nouairi I., Moschou P. N., Salem-Fnayou A. B., Mliki A., et al. (2008). Water stress induced changes in the leaf lipid composition of four grapevine genotypes with different drought tolerance. Biol. Plant. 52 161–164. 10.1007/s10535-008-0035-2 DOI
Umezawa T., Fujita M., Fujita Y., Yamaguchi-Shinozaki K., Shinozaki K. (2006). Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr. Opin. Bbiotechnol. 17 113–122. 10.1016/j.copbio.2006.02.002 PubMed DOI
Vartanian N., Marcotte L., Giraudat J. (1994). Drought rhizogenesis in Arabidopsis thaliana (differential responses of hormonal mutants). Plant Physiol. 104 761–767. 10.1104/pp.104.2.761 PubMed DOI PMC
Vítámvás P., Saalbach G., Prášil I. T., Čapková V., Opatrná J., Jahoor A. (2007). WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. J. Plant Physiol. 164 1197–1207. 10.1016/j.jplph.2006.06.011 PubMed DOI
Warnes G. R., Bolker B., Bonebakker L., Gentleman R., Liaw W., et al. (2015). gplots: Various R Programming Tools for Plotting Data. R package version 2.16.0. Available at: http://CRAN.R-project.org/package=gplots
Winfield M. O., Lu C., Wilson I. D., Coghill J. A., Edwards K. J. (2010). Plant responses to cold: transcriptome analysis of wheat. Plant Biotech. J. 8 749–771. 10.1111/j.1467-7652.2010.00536.x PubMed DOI
Xu C., Huang B. (2012). Proteins and metabolites regulated by trinexapac-ethyl in relation to drought tolerance in Kentucky bluegrass. J. Plant Growth Regul. 31 25–37. 10.1007/s00344-011-9216-x DOI
Xu D. Q., Huang J., Guo S. Q., Yang X., Bao Y. M., Tang H. J., et al. (2008). Overexpression of a TFIIIA-type zinc finger protein gene ZFP252 enhances drought and salt tolerance in rice (Oryza sativa L.). FEBS Lett. 582 1037–1043. 10.1016/j.febslet.2008.02.052 PubMed DOI
Yang J., Ordiz M. I., Jaworski J. G., Beachy R. N. (2011). Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiol. Biochem. 49 1448–1455. 10.1016/j.plaphy.2011.09.006 PubMed DOI
Yoshida T., Fujita Y., Sayama H., Kidokoro S., Maruyama K., Mizoi J., et al. (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61 672–685. 10.1111/j.1365-313X.2009.04092.x PubMed DOI
Zhang M., Ma C. Y., Lv D. W., Zhen S. M., Li X. H., Yan Y. M. (2014). Comparative phosphoproteome analysis of the developing grains in bread wheat (Triticum aestivum L.) under well-watered and water-deficit conditions. J. Proteome Res. 13 4281–4297. 10.1021/pr500400t PubMed DOI
Zhu C., Luo N., He M., Chen G., Zhu J., Yin G., et al. (2014). Molecular characterization and expression profiling of the protein disulfide isomerase gene family in Brachypodium distachyon L. PLoS ONE 9:e94704 10.1371/journal.pone.0094704 PubMed DOI PMC
Zhu Y. N., Shi D. Q., Ruan M. B., Zhang L. L., Meng Z. H., Liu J., et al. (2013). Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in cotton (Gossypium hirsutum L.). PloS One 8:e80218 10.1371/journal.pone.0080218 PubMed DOI PMC