Skip to main content
SpringerLink
Log in

Comparative analysis of barley leaf proteome as affected by drought stress

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The adaptive response of Egyptian barley land races to drought stress was analyzed using difference gel electrophoresis (DIGE). Physiological measurements and proteome alterations of accession number 15141, drought tolerant, and accession number 15163, drought sensitive, were compared. Differentially expressed proteins were subjected to MALDI-TOF-MS analysis. Alterations in proteins related to the energy balance and chaperons were the most characteristic features to explain the differences between the drought-tolerant and the drought-sensitive accessions. Further alterations in the levels of proteins involved in metabolism, transcription and protein synthesis are also indicated.

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

Similar content being viewed by others

Abbreviations

2D-PAGE:

Two-dimensional polyacrylamide gel electrophoresis

DIGE:

Difference gel electrophoresis

Hsp:

Heat shock protein

IEF:

Isoelectric focusing

RWC:

Leaf relative water content

MALDI-TOF-MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

PEA:

Plant efficiency analyzer

PI:

Performance index

PDI:

Protein disulfide isomerase

References

  • Ahmed IA (2005) Highlights of the barley breeding program in Egypt. In: Grando S, Macpherson HG (eds) Food barley: Importance, uses and local knowledge. Proceeding international workshop on food barley improvement, 14–17 January 2002, Hammamet, Tunisia. ICARDA, Aleppo, Syria, pp 1–6

  • Anjum SA, Xie X, Wang L, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agr Res 6:2026–2032

    Google Scholar 

  • Arsene F, Tomoyasu T, Bukau B (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55:3–9

    Article  PubMed  CAS  Google Scholar 

  • Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J (1999) Selective translation of cytoplasmic mRNAs in plants. Trends Plant Sci 4:142–148

    Article  PubMed  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Cazalé AC, Clement M, Chiarenza S, Roncato MA et al (2009) Altered expression of cytosolic/nuclear HSC70-1 molecular chaperone affects development and abiotic stress tolerance in Arabidopsis thaliana. J Exp Bot 60:2653–2664

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Clèment M, Leonhardt N, Droillard M, Reiter I et al (2011) The cytosolic/nuclear HSC70 and HSP90 molecular chaperones are important for stomatal closure and modulate abscisic acid-dependent physiological responses in Arabidopsis. Plant Physiol 156:1481–1492

    Article  PubMed  Google Scholar 

  • Corvey C, Koetter P, Beckhaus T, Hack J et al (2005) Carbon source-dependent assembly of the Snf1p kinase complex in Candida albicans. J Biol Chem 280:25323–25330

    Article  PubMed  CAS  Google Scholar 

  • Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130

    Article  PubMed  CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  PubMed  CAS  Google Scholar 

  • Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbó M (2006a) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Plant 127:343–352

    Article  CAS  Google Scholar 

  • Flexas J, Ribas-Carbó M, Bota J, Galmés J et al (2006b) Decreased Rubisco activity during water stress is not induced by decreased relative water content but related to conditions of low stomatal conductance and chloroplast CO2 concentration. New Phytol 172:73–82

    Article  PubMed  CAS  Google Scholar 

  • Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647

    Article  PubMed  CAS  Google Scholar 

  • Fu ZY, Zhang ZB, Liu ZH, Hu XJ, Xu P (2011) The effects of abiotic stresses on the NADP-dependent malic enzyme in the leaves of the hexaploid wheat. Biol Plant 55:196–200

    Article  CAS  Google Scholar 

  • Gao F, Zhou YJ, Zhu WP, Li XF et al (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230:1033–1046

    Article  PubMed  CAS  Google Scholar 

  • Gerrard-Wheeler MC, Arias CL, Tronconi MA, Maurino VG et al (2008) Arabidopsis thaliana NADP-malic enzyme isoforms: high degree of identity but clearly distinct properties. Plant Mol Biol 67:231–242

    Article  CAS  Google Scholar 

  • Guo P, Baum M, Grando S, Ceccarelli S 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

    Article  PubMed  CAS  Google Scholar 

  • Jedmowski C, Ashoub A, Brüggemann W (2012) Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress, evaluated by the OJIP fluorescence transient analysis. Acta Physiol Plant. doi:10.1007/s11738-012-1077-9

    Google Scholar 

  • Kotchoni SO, Bartels D (2003) Water stress induces the up-regulation of a specific set of genes in plants: aldehyde dehydrogenase as an example. Bulg J Plant Physiol, Special Issue 2003:37–51

    Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lal A, Ku MSB, Edwards GE (1996) Analysis of inhibition of photosynthesis due to water stress in the C3 species Hordeum vulgare and Vicia faba: electron transport, CO2 fixation and carboxylation capacity. Photosynth Res 49:57–69

    Article  CAS  Google Scholar 

  • Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761

    Article  PubMed  CAS  Google Scholar 

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620

    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 

  • Mèchin V, DamervalC Zivy M (2006) Total protein extraction with TCA-acetone methods. Mol Biol 355:1–8

    Article  Google Scholar 

  • Merewitz EB, Gianfagna T, Huang B (2011) Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J Exp Bot 62:5311–5333

    Article  PubMed  CAS  Google Scholar 

  • Mewes HW, Albermann K, Bähr M, Frishman D et al (1997) Overview of the yeast genome. Nature 387(Suppl. 6632):7–65

    PubMed  Google Scholar 

  • Milioni D, Hatzopoulos P (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955–961

    Article  PubMed  CAS  Google Scholar 

  • Moeder W, del Pozo O, Navarre D, Martin GB, Klessig DF (2007) Aconitase plays a role in regulating resistance to oxidative stress and cell death in Arabidopsis and Nicotiana benthamiana. Plant Mol Biol 63:273–287

    Article  PubMed  CAS  Google Scholar 

  • Narita Y, Taguchi H, Nakamura T, Ueda A et al (2004) Characterization of the salt-inducible methionine synthase from barley leaves. Plant Sci 167:1009–1016

    Article  CAS  Google Scholar 

  • Ndimba BK, Chivasa S, Simon WJ, Slabas AR (2005) Identification of Arabidopsis salt and osmotic stress responsive proteins using two dimensional difference gel electrophoresis and mass spectrometry. Proteomics 5:4185–4196

    Article  PubMed  CAS  Google Scholar 

  • Noël LD, Cagna G, Stuttmann J, Wirthmuller L et al (2007) Interaction between SGT1 and cytosolic/nuclear HSC70 chaperones regulates Arabidopsis immune responses. Plant Cell 19:4061–4076

    Article  PubMed  Google Scholar 

  • Oukarroum A, Strasser RJ (2004) Phenotyping of dark and light adapted barley plants by the fast chlorophyll a fluorescence rise OJIP. S Afr J Bot 70:277–283

    CAS  Google Scholar 

  • Oukarroum A, El Madidi S, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60:438–446

    Article  CAS  Google Scholar 

  • Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839

    Article  PubMed  CAS  Google Scholar 

  • Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle. Plant J 50:381–390

    Article  PubMed  CAS  Google Scholar 

  • Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582

    Article  PubMed  CAS  Google Scholar 

  • Rosenfeld J, Capdevielle J, Guileemot JC, Ferrara P (1992) In-gel digestion of proteins for internal sequence analysis after one or two-dimensional gel electrophoresis. Anal Biochem 203:173–179

    Article  PubMed  CAS  Google Scholar 

  • Saeedipour S (2011) Activities of sucrose-metabolizing enzymes in grains of two wheat (Triticum aestivum L.) cultivars subjected to water stress during grain filling. J Plant Breeding Crop Sci 3:106–113

    CAS  Google Scholar 

  • Shao HB, Chu LY, Jaleel CA, Manivannan P et al (2009) Understanding water deficit stress-induced changes in the basic metabolism of higher plants-biotechnologically and sustainably improving agriculture and the ecoenvironment in arid regions of the globe. Crit Rev Biotechnol 29:131–151

    Article  PubMed  CAS  Google Scholar 

  • Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858

    Article  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 

  • Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164

    Article  PubMed  CAS  Google Scholar 

  • Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  PubMed  CAS  Google Scholar 

  • Song H, Zhao R, Fan P, Wang X et al (2009) Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229:955–964

    Article  PubMed  CAS  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: The JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol 5. Kluwer Academic Publishers, The Netherlands, pp 977–980

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescent transient. In: Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security. SSARM, India, pp 72–115

    Google Scholar 

  • Swami AK, Alam SI, Sengupta N, Sarin R (2011) Differential proteomic analysis of salt stress response in Sorghum bicolor leaves. Environ Exp Bot 71:321–328

    Article  CAS  Google Scholar 

  • Talamè 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  Google Scholar 

  • Taylor L, Nunes-Nesi A, Parsley K, Leiss A et al (2010) Cytosolic pyruvate, orthophosphate dikinase functions in nitrogen remobilisation during leaf senescence and limits individual seed growth and nitrogen content. Plant J 62:641–652

    Article  PubMed  CAS  Google Scholar 

  • Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917

    Article  CAS  Google Scholar 

  • Ting JP, Willingham SB, Bergstralh DT (2008) NLRs at the intersection of cell death and immunity. Nat Rev Immunol 8:372–379

    Article  PubMed  CAS  Google Scholar 

  • Tommasini T, Svensson JT, Rodriguez EM, Wahid A 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

    Article  PubMed  CAS  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138

    Article  PubMed  Google Scholar 

  • Ueda A, Kathiresan A, Inada M, Narita Y et al (2004) Osmotic stress in barley regulates expression of a different set of genes than salt stress does. J Exp Bot 55:2213–2218

    Article  PubMed  CAS  Google Scholar 

  • Van Heerden PDR, Swanepoel JW, Kruger GHJ (2007) Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environ Exp Bot 61:124–136

    Article  Google Scholar 

  • Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Huang B (2010) Differential proteomic responses to water stress induced by PEG in two creeping bentgrass cultivars differing in stress tolerance. J Plant Physiol 167:1477–1485

    Article  PubMed  CAS  Google Scholar 

  • Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura K, Masuda A, Kuwano M, Yokota A, Akashi K (2008) Programmed proteome response for drought avoidance/tolerance in the root of a C3 xerophyte (wild watermelon) under water deficits. Plant Cell Physiol 49:226–241

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Egyptian National Gene Bank, Agricultural Research Center, for providing the seed material of the accession numbers used in this study. We would like to thank Prof. Dr. Gharib A. Gad EL-Karim at Department of Bioinformatics and Networks, AGERI, for helping in the statistical analysis carried out in this study. This study was funded by the research funding program “LOEWE—Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” of Hesse’s Ministry of Higher Education, Research, and the Arts.

Author information

Author notes

  1. Ahmed Ashoub

    Present address: Institute of Ecology, Evolution, and Diversity, Johann Wolfgang Goethe-University Frankfurt, Max-von-Laue Str. 13, 60438, Frankfurt am Main, Germany

Authors and Affiliations

  1. Biodiversity and Climate Research Centre (BiK-F), Frankfurt am Main, Germany

    Ahmed Ashoub, Thomas Berberich & Wolfgang Brüggemann

  2. Agricultural Genetic Engineering Research Institute (AGERI), ARC, Giza, Egypt

    Ahmed Ashoub

  3. Institute of Pharmaceutical Chemistry, Johann Wolfgang Goethe-University Frankfurt, Frankfurt am Main, Germany

    Tobias Beckhaus & Michael Karas

  4. Institute of Ecology, Evolution, and Diversity, Johann Wolfgang Goethe-University Frankfurt, Max-von-Laue Str. 13, 60438, Frankfurt am Main, Germany

    Wolfgang Brüggemann

Authors
  1. Ahmed Ashoub
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tobias Beckhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Berberich
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael Karas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wolfgang Brüggemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed Ashoub.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ashoub, A., Beckhaus, T., Berberich, T. et al. Comparative analysis of barley leaf proteome as affected by drought stress. Planta 237, 771–781 (2013). https://doi.org/10.1007/s00425-012-1798-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1798-4

Keywords

Search

Navigation