Abstract
Low water availability is the major environmental factor limiting crop productivity. Transcriptome analysis was used to study terminal drought response in wild emmer wheat, Triticum dicoccoides, genotypes contrasting in their productivity and yield stability under drought stress. A total of 5,892 differentially regulated transcripts were identified between drought and well-watered control and/or between drought resistant (R) and drought susceptible (S) genotypes. Functional enrichment analyses revealed that multilevel regulatory and signalling processes were significantly enriched among the drought-induced transcripts, in particular in the R genotype. Therefore, further analyses were focused on selected 221 uniquely expressed or highly abundant transcripts in the R genotype, as potential candidates for drought resistance genes. Annotation of the 221 genes revealed that 26% of them are involved in multilevel regulation, including: transcriptional regulation, RNA binding, kinase activity and calcium and abscisic acid signalling implicated in stomatal closure. Differential expression patterns were also identified in genes known to be involved in drought adaptation pathways, such as: cell wall adjustment, cuticular wax deposition, lignification, osmoregulation, redox homeostasis, dehydration protection and drought-induced senescence. These results demonstrate the potential of wild emmer wheat as a source for candidate genes for improving drought resistance.
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References
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signalling. Plant Cell 15:63–78
Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L (2009) Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics 10:279
Araus JL, Slafer GA, Royo C, Dolores SM (2008) Breeding for yield potential and stress adaptation in cereal. Crit Rev Plant Sci 27:377–412
Asseng S, Van Herwaarden A (2003) Analysis of the benefits to wheat yield from assimilates stored prior to grain filling in a range of environments. Plant Soil 256:217–229
Avneri A (2009) Drought resistance and water use efficiency in wild emmer wheat (Triticum turgidum ssp. dicoccoides). M.Sc. dissertation, the Robert H. Smith Faculty of Agriculture Food and Environment, The Hebrew University of Jerusalem. (Hebrew with English abstract)
Barbazuk WB, Fu Y, McGinnis KM (2008) Genome-wide analyses of alternative splicing in plants: opportunities and challenges. Genome Res 18:1381–1392
Barrs C, Weatherley PE (1968) A re-examination of the relative turgidity technique for estimating water deficit in leaves. Austr J of Biol Sci 15:413–428
Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58
Batistic O, Kudla J (2004) Integration and channeling of calcium signalling through the CBL calcium sensor/CIPK protein kinase network. Planta 219:915–924
Benjamins R, Malenica N, Luschnig C (2005) Regulating the regulator: the control of auxin transport. BioEssays 27:1246–1255
Bernier F, Berna A (2001) Germins and germin-like proteins: plant do-all proteins. But what do they do exactly? Plant Physiol Biochem 39:545–554
Blum A (1988) Plant Breeding for Stress Environments. CRC, Boca Raton
Blum A (2005) Drought resistance, water-use efficiency, and yield potential-are they compatible, dissonant, or mutually exclusive? Aust J Agric Res 56:1159–1168
Boyer J (1982) Plant productivity and environment. Science 218:443–448
Boyer J, Westgate M (2004) Grain yields with limited water. J Exp Bot 55:2385–2394
Cameron KD, Teece MA, Smart LB (2006) Increased accumulation of cuticular wax and expression of lipid transfer protein in response to periodic drying events in leaves of tree tobacco. Plant Physiol 140:176–183
Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14
Chao WS, Gu YQ, Pautot V, Bray EA, Walling LL (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120:979–992
Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139
Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of muclear hexokinase1 complex in glucose signalling. Cell 127:579–589
Choi DW, Zhu B, Close T (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
Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture–not by affecting ATP synthesis. Trends Plant Sci 5:187–188
Cui X, Churchill GA (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biol 4:210.1–210.10
D'Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K (2006) Alternative complex formation of the Ca+2 - regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872
Degenkolbe T, Do PT, Zuther E, Repsilber D, Walther D, Hincha DK, Kohl KI (2009) Expression profiling of rice cultivars differing in their tolerance to long-term drought stress. Plant Mol Biol 69:133–153
Diab AA, Teulat-Merah B, This D, Ozturk NZ, Benscher D, Sorrells ME (2004) Identification of drought-inducible genes and differentially expressed sequence tags in barley. Theor Appl Genet 109:1417–1425
Diab AA, Kantety R, Ozturk N, Benscher D, Nachit M, Sorrells M (2008) Drought-inducible genes and differentially expressed sequence tags associated with components of drought tolerance in durum wheat. Sci Res Essay 3:9–27
Deyholos MK (2010) Making the most of drought and salinity transcriptomeics. Plant Cell Environ 33:648–654
Dunwell JM, Gibbings JG, Mahmood T, Naqvi SMS (2008) Germin and germin-like proteins: evolution, structure, and function. Crit Rev Plant Sci 27:342–375
Egawa C, Kobayashi F, Ishibashi M, Nakamura T, Nakamura C, Takumi S (2006) Differential regulation of transcript accumulation and alternative splicing of a DREB2 homolog under abiotic stress conditions in common wheat. Genes Genet Sys 81:77–91
Ergen NZ, Thimmapuram J, Bohnert HJ, Budak H (2009) Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics 9:377–396
Fahima T, Röder MS, Wendehake K, Kirzhner VM, Nevo E (2002) Microsatellite polymorphism in natural populations of wild emmer wheat, Triticum dicoccoides, in Israel. Theor Appl Genet 104:17–29
Feldman M (2001) The origin of cultivated wheat. In: Bonjean A, Angus W (eds) The world wheat book. Lavoisier Technical and Doc, Paris, pp 3–56
Feldman M, Sears ER (1981) The wild gene resources of wheat. Sci Am 244:102–112
Feuillet C, Eversole K (2007) Physical mapping of the wheat genome: a coordinated effort to lay the foundation for genome sequencing and develop tools for breeders. Isr J Plant Sci 55:307–313
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. The Plant Cell 12:599–610
Fischer RA, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield responses. Aust J Agri Res 29:879–912
Fresneau C, Ghashghaie J, Cornic G (2007) Drought effect on nitrate reductase and sucrose-phosphate synthase activities in wheat (Triticum durum L.): role of leaf internal CO2. J Exp Bot 58:2983–2992
Froman BE, Edwards PC, Bursch AG, Dehesh K (2000) ACX3, a novel medium-chain Acyl-Coenzyme a oxidase from Arabidopsis. Plant Physiol 123:733–742
Gan S, Amasino RM (1997) Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiol 113:313–319
Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157
Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat (Triticum aestivum L.). Plant Biotech J 5:192–206
Gulick PJ, Drouin S, Yu Z, Danyluk J, Poisson G, Monroy AF, Sarhan F (2005) Transcriptome comparison of winter and spring wheat responding to low temperature. Genome 48:913–923
Guo P, Baum M, Grando S, Ceccarelli S, Bai G, Li R, von Korff M, Varshney RK, Graner A, Valkoun J (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
Habash D, Kehel Z, Nachit M (2009) Genomic approaches for designing durum wheat ready for climate change with a focus on drought. J Exp Bot 60:2805–2815
Halford NG, Hey S, Jhurreea D, Laurie S, McKibbin RS, Paul M, Zhang Y (2003) Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J Exp Bot 54:467–475
Hochberg Y (1988) A sharper Bonferroni procedure for multiple tests of significance. Biomet 75:800–803
Hu WJ, Kawaoka A, Tsai CJ, Lung J, Osakabe K, Ebinuma H, Chiang VL (1998) Compartmentalized expression of two structurally and functionally distinct 4-coumarate: CoA ligase genes in aspen (Populus tremuloides). Proc Nat Acad Sci 95:5407–5412
Hu H, Dai M, Yao J, Xiao B, Li X, Zhang Q, Xiong L (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992
Huang D, Wu W, Abrams SR, Cutler AJ (2008a) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3307
Huang J, Wang MM, Bao YM, Sun SJ, Pan LJ, Zhang HS (2008b) SRWD: a novel WD40 protein subfamily regulated by salt stress in rice (Oryza sativa L.). Gene 424:71–79
Jamet E, Canut H, Boudart G, Pont-Lezica RF (2006) Cell wall proteins: a new insight through proteomics. Trends Plant Sci 11:33–39
Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:25
Jiang Y, Yang B, Deyholos MK (2009) Functional characterization of the Arabidopsis bHLH92 transcription factor in abiotic stress. Mol Genet Genomics 282:503–516
Jouannic N, Lepetit M, Vergnolle C, Cantrel C, Gardies AM, Kader JC, Arondel V (1998) Isolation of cDNA from Arabidopsis thaliana that complements the sec14 mutant of yeast. Eur J Biochem 258:402–410
Joung JG, Corbett AM, Fellman SM, Tieman DM, Klee HJ, Giovannoni JJ, Fei Z (2009) Plant MetGenMAP: an integrative analysis system for plant systems biology. Plant Physiol 151:1758–1768
Kandel S, Sauveplane V, Olry A, Diss L, Benveniste I, Pinot F (2006) Cytochrome P450-dependent fatty acid hydroxylases in plants. Phytochem Rev 5:359–372
Kawaguchi R, Girke T, Bray EA, Bailey-Serres J (2004) Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant J 38:823–839
Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656
Ladizinsky G (1998) Plant Evolution under Domestication. Kluwer, Dordrecht
Lee Y, Bak G, Choi Y, Chuang WI, Cho HT, Lee Y (2008) Roles of phosphatidylinositol 3-kinase in root hair growth. Plant Physiol 147:624–635
Lin WH, Ye R, Ma H, Xu ZH, Xue HW (2004) DNA chip-based expression profile analysis indicates involvement of the phosphatidylinositol signalling pathway in multiple plant responses to hormone and abiotic treatments. Cell Res 14:34–45
Lintala M, Allahverdiyeva Y, Kangasjarvi S, Lehtimaki N, Keranen M, Rintamaki E, Aro EM, Mulo P (2009) Comparative analysis of leaf-type ferredoxin-NADP oxidoreductase isoforms in Arabidopsis thaliana. Plant J 57:1103–1115
Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280:1943–1945
Loss S, Siddique K (1994) Morphological and physiological traits associated with wheat yield increases in Mediterranean environments. Adv Agron 52:229–276
Lu PL, Chen NZ, An R, Su Z, Qi BS, Ren F, Chen J, Wang XC (2007) A novel drought-inducible gene, ATAF1, encodes a NAC family protein that negatively regulates the expression of stress-responsive genes in Arabidopsis. Plant Mol Biol 63:289–305
Luan S (2008) The CBL–CIPK network in plant calcium signalling. Trends Plant Sci 14:37–42
Lumbreras V, Albà MM, Kleinow T, Koncz C, Pagès M (2001) Domain fusion between SNF1-related kinase subunits during plant evolution. EMBO Rep 2:55
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068
Mane SP, Vasquez-Robinet C, Sioson AA, Heath LS, Grene R (2007) Early PLD α -mediated events in response to progressive drought stress in Arabidopsis: a transcriptome analysis. J Exp Bot 58:241–252
Mazzucotelli E, Mastrangelo AM, Crosatti C, Guerra D, Stanca AM, Cattivelli L (2008) Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci 174:420–431
McFadden E, Sears E (1946) The origin of Triticum spelta and its free-threshing hexaploid relatives. J Hered 37(81–89):106–116
Miyazono K, Miyakawa T, Sawano Y, Kubota K, Kang HJ, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y (2009) Structural basis of abscisic acid signalling near-final version. Nature 3(462):609–614
Monks DE, Aghoram K, Courtney PD, DeWald DB, Dewey R (2001) Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2. Plant Cell 13:1205–1219
Monroy AF, Dryanova A, Malette B, Oren DH, Ridha Farajalla M, Liu W, Danyluk J, Ubayasena LW, Kane K, Scoles GJ, Sarhan F, Gulick PJ (2007) Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Mol Biol 64:409–423
Moore JP, Vicre-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plantarum 134:237–245
Morey JS, Ryan JC, Van Dolah FM (2006) Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol Proced Online 8:175–193
Munne-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216
Nakashima K, Tran LSP, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (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
Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95
Nevo E, Korol AB, Beiles A, Fahima T (2002) Evolution of Wild Emmer and Wheat Improvement: Population Genetics, Genetic Resources and Genome Organization of Wheat’s Progenitor, Triticum dicoccoides. Springer, Heidelberg
Ono K, Nishi Y, Watanabe A, Terashima I (2001) Possible mechanisms of adaptive leaf senescence. Plant Biol (Stuttg) 3:234–243
Ozturk ZN, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert HJ (2002) Monitoring large-scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573
Palma JM, Sandalio LM, Javier Corpas F, Romero-Puertas MC, McCarthy I, del Río LA (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40:521–530
Pandey GK (2008) Emergence of a novel calcium signalling pathway in plants: CBL-CIPK signalling network. Physiol and Mol Biol of Plants 14:51–68
Park KY, Jung JY, Park J, Hwang JU, Kim YW, Hwang I, Lee Y (2003) A role for phosphatidylinositol 3-phosphate in abscisic acid-induced reactive oxygen species generation in guard cells. Plant Physiol 132:92–98
Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TF (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071
Pastori GM, Foyer CH (2002) Common components, networks, and pathways of cross-tolerance to stress. the central role of “redox” and abscisic acid-mediated controls. Plant Physiol 129:460–468
Peleg Z, Fahima T, Abbo S, Krugman T, Nevo E, Yakir D, Saranga Y (2005) Genetic diversity for drought resistance in wild emmer wheat and its ecogeographical associations. Plant Cell Environ 28:176–191
Peleg Z, Fahima T, Saranga Y (2007) Drought resistance in wild emmer wheat: physiology, ecology and genetics. Isr J Plant Sci 55:289–297
Peleg Z, Saranga Y, Krugman T, Abbo S, Nevo E, Fahima T (2008a) Allelic diversity associated with aridity gradient in wild emmer wheat populations. Plant Cell Environ 31:39–49
Peleg Z, Saranga Y, Yazici AM, Fahima T, Ozturk L, Cakmak I (2008b) Grain zinc, iron and protein concentrations and zinc-efficiency in wild emmer wheat under contrasting irrigation regimes. Plant Soil 306:57–67
Poole R, Barker G, Wilson ID, Coghill JA, Edwards KJ (2007) Measuring global gene expression in polyploidy; a cautionary note from allohexaploid wheat. Funct Integr Genomics 7:207–219
Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9:432
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202
Reiter WD (2002) Biosynthesis and properties of the plant cell wall. Curr Opin Plant Biol 5:536–542
Richardson A, Boscari A, Schreiber L, Kerstiens G, Jarvis M, Herzyk P, Fricke W (2007) Cloning and expression analysis of candidate genes involved in wax deposition along the growing barley (Hordeum vulgare) leaf. Planta 226:1459–1473
Ringli C, Keller B, Ryser U (2001) Glycine-rich proteins as structural components of plant cell walls. Cell Mol Life Sci (CMLS) 58:1430–1441
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636
Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1380–1393
Robert HS, Offringa R (2008) Regulation of auxin transport polarity by AGC kinases. Curr Opin Plant Biol 11:495–502
Saibo NJM, Lourenco T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103:609–623
Schafleitner R, Gutierrez Rosales RO, Gaudin A, Alvarado Aliaga CA, Martinez GN, Tincopa Marca LR, Bolivar LA, Delgado FM, Simon R, Bonierbale M (2007) Capturing candidate drought tolerance traits in two native Andean potato clones by transcription profiling of field grown plants under water stress. Plant Physiol Biochem 45:673–690
Schreiber AW, Sutton T, Caldo RA, Kalashyan E, Lovell B, Mayo G, Muehlbauer GJ, Druka A, Waugh R, Wise RP, Langridge P, Baumann U (2009) Comparative transcriptomeics in the Triticeae. BMC Genomics 10:285
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302
Seki M, Okamoto M, Matsui A, Kim JM, Kurihara Y, Ishida J, Morosawa T, Kawashima M, To TK, Shinozaki K (2009) Microarray analysis for studying the abiotic stress responses in plants. In: Jain SM, Brar DS (eds) Molecular Techniques in Crop Improvement. Springer, Norwell, pp 333–355
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends Plant Sci 7:41–48
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417
Sibout R, Eludes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Seguin A (2005) Cinnamyl alcohol dehydrogenase C and-D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell Online 17:2059–2076
Skern R, Frost P, Nilsen F (2005) Relative transcript quantification by quantitative PCR: roughly right or precisely wrong? BMC Mol Biol 6:10
Suprunova T, Krugman T, Fahima T, Chen G, Shams I, Korol A, Nevo E (2004) Differential expression of dehydrin genes in wild barley, Hordeum spontaneum, associated with resistance to water deficit. Plant Cell Environ 27:1297–1308
Suprunova T, Krugman T, Distelfeld A, Fahima T, Nevo E, Korol A (2007) Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley. Plant Mol Biol 64:17–34
Swarup R, Bennett M (2003) Auxin transport: the fountain of life in plants? Dev Cell 5:824–826
Talame V, Ozturk NZ, Bohnert HJ, Tuberosa R (2007) Barley transcript profiles under dehydration shock and drought stress treatments: a comparative analysis. J Exp Bot 58:229–240
Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: unlocking genetic potential from the wild. Science 277:1063–1066
Turner NC, Asseng S (2005) Productivity, sustainability, and rainfall-use efficiency in Australian rainfed Mediterranean agricultural systems. Aust J Agric Res 56:1123–1136
Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc Natl Acad Sci USA 106(41):17588–17593. doi:10.1073/pnas.0907095106
V'ery AA, Sentenac H (2003) Molecular mechanisms and regulation of K+ transport in higher plants. Ann Rev Plant Biol 54:575–603
van Nocker S, Ludwig P (2003) The WD-repeat protein superfamily in Arabidopsis conservation and divergence in structure and function. BMC Genomics 4:50
Vinocur B, Altman A (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechol 16:123–132
Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative Growth Stage. Plant Physiol 139:822–835
Wang Z, Wang F, Duan R, Liu JY (2007) Purification and physicochemical characterization of a recombinant phospholipid hydroperoxide glutathione peroxidase from Oryza sativa. J Biochem Mol Biol 40:412–418
Ward JH Jr (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244
Welti R, Wang X (2004) Lipid species profiling: a high-throughput approach to identify lipid compositional changes and determine the function of genes involved in lipid metabolism and signalling. Curr Opin Plant Biol 7:337–344
Whittaker A, Bochicchio A, Vazzana C, Lindsey G, Farrant J (2001) Changes in leaf hexokinase activity and metabolite levels in response to drying in the desiccation-tolerant species Sporobolus stapfianus and Xerophyta viscosa. J Exp Bot 52:961–969
Xu X, Dietrich CR, Delledonne M, Xia Y, Wen TJ, Robertson DS, Nikolau BJ, Schnable PS (1997) Sequence analysis of the cloned glossy8 gene of maize suggests that it may code for a β-ketoacyl reductase required for the biosynthesis of cuticular waxes. Plant Physiol 115:501–510
Xue GP, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R (2008) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454
Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473
Zadoks JC, Chang TT, Konzak CF (1974) Decimal code for growth stages of cereals. Weed Res 14:415–421
Zhang H, Whitelegge JP, Cramer WA (2001) Ferredoxin: NADP oxidoreductase is a subunit of the chloroplast cytochrome b6f complex. J Biol Chem 276:38159–38165
Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res 97:111–119
Acknowledgment
This project was supported by the Programme for Sustainable Agriculture funded by the Israel Ministry of Science (# 01-21-00048), the French Ministry for Foreign Affairs and the French Ministry for Education and Research; we also acknowledge The Israel Science Foundation grant #1089/04 and equipment grants #048/99 and 1478/04. Z. Peleg is indebted to the Israel Council for the Higher Education postdoctoral fellowships award. The authors thank A. Fahum, M. Goldshmit, S. Chalifa and Y. Jun for their excellent technical assistance.
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Krugman, T., Chagué, V., Peleg, Z. et al. Multilevel regulation and signalling processes associated with adaptation to terminal drought in wild emmer wheat. Funct Integr Genomics 10, 167–186 (2010). https://doi.org/10.1007/s10142-010-0166-3
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DOI: https://doi.org/10.1007/s10142-010-0166-3