Skip to main content
SpringerLink
Log in

Transcriptome pathways unique to dehydration tolerant relatives of modern wheat

  • Original Paper
  • Published:
Functional & Integrative Genomics Aims and scope Submit manuscript

Abstract

Among abiotic stressors, drought is a major factor responsible for dramatic yield loss in agriculture. In order to reveal differences in global expression profiles of drought tolerant and sensitive wild emmer wheat genotypes, a previously deployed shock-like dehydration process was utilized to compare transcriptomes at two time points in root and leaf tissues using the Affymetrix GeneChip® Wheat Genome Array hybridization. The comparison of transcriptomes reveal several unique genes or expression patterns such as differential usage of IP3-dependent signal transduction pathways, ethylene- and abscisic acid (ABA)-dependent signaling, and preferential or faster induction of ABA-dependent transcription factors by the tolerant genotype that distinguish contrasting genotypes indicative of distinctive stress response pathways. The data also show that wild emmer wheat is capable of engaging known drought stress responsive mechanisms. The global comparison of transcriptomes in the absence of and after dehydration underlined the gene networks especially in root tissues that may have been lost in the selection processes generating modern bread wheats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Araus JL, Ferrio JP, Buxo R, Voltas J (2007) The historical perspective of dryland agriculture: lessons learned from 10 000 years of wheat cultivation. J Exp Bot 58:131–145

    Article  PubMed  CAS  Google Scholar 

  • Barnabas B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38

    PubMed  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Bohnert HJ, Gong Q, Li P, Ma S (2006) Unraveling abiotic stress tolerance mechanisms—getting genomics going. Curr Opin Plant Biol 9:180–188

    Article  PubMed  CAS  Google Scholar 

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    Article  PubMed  CAS  Google Scholar 

  • Cebeci O, Kokturk B, Ergen N, Ozturk L, Cakmak I, Budak H (2008) Differential expression of wheat transcriptomes in response to varying cadmium concentrations. Biol Plant 52:703–708

    Article  CAS  Google Scholar 

  • Chao S, Lazo GR, You F, Crossman CC, Hummel DD, Lui N, Laudencia-Chingcuanco D, Anderson JA, Close TJ, Dubcovsky J, Gill BS, Gill KS, Gustafson JP, Kianian SF, Lapitan NLV, Nguyen HT, Sorrells ME, McGuire PE, Qualset CO, Anderson OD (2006) Use of large-scale Triticeae expressed sequence tag resource to reveal gene expression profiles in hexaploid wheat (Triticum aestivum L.). Genome 49:531–544

    Article  PubMed  Google Scholar 

  • Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147:469–486

    Article  PubMed  CAS  Google Scholar 

  • Cramer GR, Ergul A, Grimplet J, Tillett RL, Tattersall EAR, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134

    Article  PubMed  CAS  Google Scholar 

  • Cseke L, Dudoreva N, Pichersky E (1998) Structure and evolution of linalool synthase. Mol Biol Evol 15:1491–1498

    PubMed  CAS  Google Scholar 

  • Deuschle K, Funck D, Hellman H, Dascher K, Binder S, Frommer W (2001) A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity. Plant J 27:345–355

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploidy wheat under domestication. Science 316:1862–1866

    Article  PubMed  CAS  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Ergen ZN, Budak H (2009) Sequencing over 13, 000 ESTs from six subtractive cDNA libraries of wild and modern wheats following slow drought stress. Plant Cell Environ 32:220–236

    Article  PubMed  CAS  Google Scholar 

  • Ergen ZN, Dinler G, Shearman RC, Budak H (2007) Identifying cloning and structural analysis of differentially expressed genes upon Puccinia infection of Festuca rubra var. rubra. Gene 393:145–152

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  PubMed  CAS  Google Scholar 

  • Guy C, Porat R, Hurry V (2006) Plant cold and abiotic stress gets hot. Physiol Plant 126:1–4

    Article  CAS  Google Scholar 

  • Higuchi K, Suzuki K, Nakanishi H, Yamaguchi H, Nishizawa NK, Mori S (1999) Cloning nicotianamine synthase genes, novel genes involved in the biosynthesis of phytosiderophores. Plant Physiol 119:471–479

    Article  PubMed  CAS  Google Scholar 

  • Higuchi K, Watanabe S, Takahashi M, Kawasaki S, Nakanishi H, Nishizawa NK, Mori S (2001) Nicotianamine synthase gene expression differs in barley and rice under Fe-deficient conditions. Plant J 25:159–167

    Article  PubMed  CAS  Google Scholar 

  • Jones HG (2007) Monitoring plant and soil water statues: established and novel methods revisited and their relevance to studies of drought tolerance. J Exp Bot 58:199–130

    Article  Google Scholar 

  • Kaldenhoff R, Carbo MR, Sans JF, Lovisolo C, Heckwolf M, Norbert U (2008) Aquaporins and plant water balance. Plant Cell Environ 31:658–666

    Article  PubMed  CAS  Google Scholar 

  • Kaur N, Gupta AK (2005) Signal transduction pathways under abiotic stresses in plants. Curr Sci 88:1771–1780

    CAS  Google Scholar 

  • Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Rao S, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Langridge P, Paltridge N, Fincher G (2006) Functional genomics of abiotic stress tolerance in cereals. Brief Funct Genomic Proteomic 4:343–354

    Article  PubMed  CAS  Google Scholar 

  • Lee YH, Chun JY (1998) A new homeodomain-leucine zipper gene from Arabidopsis thaliana induced by water stress and abscisic acid treatment. Plant Mol Biol 37:377–384

    Article  PubMed  CAS  Google Scholar 

  • Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane-bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433

    Article  PubMed  Google Scholar 

  • Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, Naylor RL (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319:607–610

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Mohammadi M, Kav NNV, Deyholos MK (2007) Transcriptional profiling of hexaploid wheat (Triticum aestivum L.) roots identifies novel, dehydration-responsive genes. Plant Cell Environ 30:630–645

    Article  PubMed  CAS  Google Scholar 

  • Muller PY, Janovjak H, Miserez AR, Dobbie Z (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 32:1372–1379

    PubMed  CAS  Google Scholar 

  • Munns R, James RA, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  PubMed  CAS  Google Scholar 

  • Olsen AN, Ernst HA, Lo Leggio L, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  PubMed  CAS  Google Scholar 

  • Ormeno E, Mevy JP, Vila B, Bousquet-Melou A, Greff S, Bonin G, Fernandez C (2007) Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential. Chemosphere 67:276–284

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Poustini K, Siosemardeh A, Ranjbar M (2007) Proline accumulation as a response to salt stress in 30 wheat (Triticum aestivum L.) cultivars differing in salt tolerance. Genet Resour Crop Evol 54:925–934

    Article  CAS  Google Scholar 

  • Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151

    Article  PubMed  CAS  Google Scholar 

  • Rampino P, Pataleo S, Gerardi C, Mita G, Perrotta C (2006) Drought stress response in wheat: physiological and molecular analysis of tolerant and sensitive genotypes. Plant Cell Environ 29:2143–2152

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Uribe L, O'Connell MA (2006) A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris). J Exp Bot 57:1391–1398

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  PubMed  CAS  Google Scholar 

  • Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003) An EREBP/AP2-type protein Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106:923–930

    PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • The Gene Ontology Consortium (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  Google Scholar 

  • Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix–loop–helix transcription factor family. Plant Cell 15:1749–1770

    Article  PubMed  CAS  Google Scholar 

  • Vasil IK (2007) Molecular genetic improvement of cereals: transgenic wheat (Triticum aestivum L.). Plant Cell Rep 26:1133–1154

    Article  PubMed  CAS  Google Scholar 

  • Vinocur B, Altman R (2005) Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 16:123–132

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(Suppl):S165–S183

    PubMed  CAS  Google Scholar 

  • Xue GP, McIntyre LC, Glassop D, Shorter R (2008) Use of expression analysis to dissect alterations in carbohydrate metabolism in wheat leaves during drought stres. Plant Mol Biol 67:197–214

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Wang X, Jiao Y, Qin Y, Liu X, He K, Chen C, Ma L, Wang J, Xiong L, Zhang Q, Fan L, Deng XW (2007) Global genome expression analysis of rice in response to drought and high-salinity stresses in shoot, flag leaf, and panicle. Plant Mol Biol 63:591–608

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Ay-Ka Ltd Company for allowing the use of Partek® Genomics Suite version 6.3 Beta (Partek Incorporated) and T. Unver for help in making Tables 2 and 3. This work was partially supported by EU-FP6 COST Action and TUBITAK (The Scientific and Technological Research Council of Turkey).

Author information

Authors and Affiliations

  1. Biological Sciences & Bioengineering Program, Faculty of Engineering and Natural Sciences, Sabanci University, Tuzla, Istanbul, 34956, Turkey

    Neslihan Z. Ergen & Hikmet Budak

  2. Roy J. Carver Biotechnology Center, University of Illinois at Urbana–Champaign, 1206 W Gregory Drive, Urbana, IL, 61801, USA

    Jyothi Thimmapuram

  3. Department of Plant Biology and Department of Crop Sciences, University of Illinois at Urbana–Champaign, 192 ERML, 1201 W. Gregory Drive, Urbana, IL, 61801, USA

    Hans J. Bohnert

Authors
  1. Neslihan Z. Ergen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jyothi Thimmapuram
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hans J. Bohnert
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hikmet Budak
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hikmet Budak.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Supplementary Table S1

List of probes with inverse differential regulation in response to quickly imposed and severe water loss between contrasting genotypes. a After 4 h in leaf, b after 8 h in leaf, c after 4 h in root, and d after 8 h in root tissues. The dataset contains probes with p < 0.01 and DE < −3 or >3. Given are fold changes calculated by ANOVA. Only probes with significant expression changes in both genotypes and time points are included. “No hits” and “unclassified” proteins are excluded from the probe sets that are outlined. Up-regulation, as fold change, is highlighted with bold characters, whereas down-regulation fold changes by are set to italics. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (highlighted with red characters) (DOC 72 KB)

Supplementary Table S2

List of stress responsive probes expressed in the absence of dehydration a in the leaf and b root tissues of the contrasting genotypes. The dataset contains probes with p < 0.01 and DE < −3 or >3. Empty cells indicate no significant differential regulation. Given are fold changes calculated by ANOVA. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (highlighted with red characters) (DOC 17 KB)

Supplementary Table S3

Lists of differentially expressed probes. Dataset contains probes with p < 0.01 and DE <−3 or >3. p values and fold changes are calculated by ANOVA. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (XLS 2.19 MB)

Supplementary Table S4

Self annotation and data used for annotation of differentially expressed probe sets. Data for three approaches used for annotations of the drought responsive probes are given in separate worksheets with appropriate titles: HarvEST (http://harvest.ucr.edu); nucleotide BLAST results are BLASTn (Altschul 1997) hits to the TC collections of wheat, barley, maize, rice, rye, and sorghum available in the TIGR database (http://www.tigr.org), the GenBank nr database (http://www.ncbi.nlm.nih.gov), and in the Arabidopsis genome database (http://www.arabidopsis.org), and protein BLAST results are BLASTx (Altschul 1997) hits to the Poaceae database (http://www.gramene.org). Tables were prepared by parsing the number one hits with cutoff e values less than 0.00001. Comparison of self-annotations with annotations downloaded from NetAffyx Analysis Center for probes with differential regulation (http://www.affymetrix.com/analysis/index.affx) are given in Annotations worksheet (XLS 10.2 MB)

Supplementary Table S5

Lists of common probes in genotypes, tissues, or time of shock-like dehydration. The dataset contains probes with p < 0.01 and DE <−3 or >3. p values and fold changes are calculated by ANOVA. Only probes with differential expression in both genotypes and time points were included in the analysis. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (XLS 319 KB)

Supplementary Table S6

Lists of differentially expressed probes in non-stressed tissues. The dataset contains probes with p < 0.01 and DE <−3 or >3. p values and fold changes are calculated by ANOVA. Only stress-responsive probes with differential expression in both time points were included to analysis. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (XLS 251 KB)

Supplementary Table S7

Shock-like dehydration response of selected protein families. The dataset contains probes with p < 0.01 and DE <−3 or >3. p values and fold changes are calculated by ANOVA. Up-regulation, as fold change, is highlighted with bold characters, whereas down-regulation fold changes are in italics. TR tolerant genotype TR39477, TS sensitive genotype TTD-22. Differential regulation in aquaporins, ROS scavenging through glutathione and LEA, dehydrin, and compatible solutes are given in separate worksheets (XLS 26 KB)

Supplementary Fig. S1

Treeview of all probes with differential regulation in leaf tissues. Color saturation reflects the fold change, where green indicates >3-fold down-regulated and red >3-fold up-regulated probes at p < 0.01. Missing probes with no significant differential regulation are marked with dark gray. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (GIF 12.4 MB)

High resolution image file (TIFF 1.65 MB)

Supplementary Fig. S2

Treeview of all probes with differential regulation in root tissues. Color saturation reflects the fold change, where green indicates >3-fold down-regulated and red >3-fold up-regulated probes at p < 0.01. Missing probes with no significant differential regulation are marked dark gray. TR tolerant genotype TR39477, TS sensitive genotype TTD-22 (GIF 12.1 MB)

High resolution image file (TIFF 1.63 MB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ergen, N.Z., Thimmapuram, J., Bohnert, H.J. et al. Transcriptome pathways unique to dehydration tolerant relatives of modern wheat. Funct Integr Genomics 9, 377–396 (2009). https://doi.org/10.1007/s10142-009-0123-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10142-009-0123-1

Keywords

Search

Navigation