Planta

, Volume 237, Issue 3, pp 771–781 | Cite as

Comparative analysis of barley leaf proteome as affected by drought stress

  • Ahmed Ashoub
  • Tobias Beckhaus
  • Thomas Berberich
  • Michael Karas
  • Wolfgang Brüggemann
Original Article

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.

Keywords

Barley Difference gel electrophoresis (DIGE) Drought stress Fv/Fm MALDI-TOF-MS Performance index Proteome analysis 

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

  1. 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 1–6Google Scholar
  2. 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 6:2026–2032Google Scholar
  3. Arsene F, Tomoyasu T, Bukau B (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55:3–9PubMedCrossRefGoogle Scholar
  4. 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 62:3049–3059PubMedCrossRefGoogle Scholar
  5. Bailey-Serres J (1999) Selective translation of cytoplasmic mRNAs in plants. Trends Plant Sci 4:142–148PubMedCrossRefGoogle Scholar
  6. Boyer JS (1982) Plant productivity and environment. Science 218:443–448PubMedCrossRefGoogle Scholar
  7. Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  8. 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 60:2653–2664PubMedCrossRefGoogle Scholar
  9. 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 120:979–992PubMedCrossRefGoogle Scholar
  10. 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 156:1481–1492PubMedCrossRefGoogle Scholar
  11. 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 280:25323–25330PubMedCrossRefGoogle Scholar
  12. Fitzgerald TL, Waters DLE, Henry RJ (2009) Betaine aldehyde dehydrogenase in plants. Plant Biol 11:119–130PubMedCrossRefGoogle Scholar
  13. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189PubMedCrossRefGoogle Scholar
  14. 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 127:343–352CrossRefGoogle Scholar
  15. 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 172:73–82PubMedCrossRefGoogle Scholar
  16. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Annu Rev Biochem 70:603–647PubMedCrossRefGoogle Scholar
  17. 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 55:196–200CrossRefGoogle Scholar
  18. Gao F, Zhou YJ, Zhu WP, Li XF et al (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230:1033–1046PubMedCrossRefGoogle Scholar
  19. 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 67:231–242CrossRefGoogle Scholar
  20. 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 60:3531–3544PubMedCrossRefGoogle Scholar
  21. 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
  22. 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 2003:37–51Google Scholar
  23. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349CrossRefGoogle Scholar
  24. Krishna P, Gloor G (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones 6:238–246PubMedCrossRefGoogle Scholar
  25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  26. 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 49:57–69CrossRefGoogle Scholar
  27. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146:748–761PubMedCrossRefGoogle Scholar
  28. Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620PubMedCrossRefGoogle Scholar
  29. Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158PubMedCrossRefGoogle Scholar
  30. Mèchin V, DamervalC Zivy M (2006) Total protein extraction with TCA-acetone methods. Mol Biol 355:1–8CrossRefGoogle Scholar
  31. 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 62:5311–5333PubMedCrossRefGoogle Scholar
  32. Mewes HW, Albermann K, Bähr M, Frishman D et al (1997) Overview of the yeast genome. Nature 387(Suppl. 6632):7–65PubMedGoogle Scholar
  33. Milioni D, Hatzopoulos P (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol Biol 35:955–961PubMedCrossRefGoogle Scholar
  34. 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 63:273–287PubMedCrossRefGoogle Scholar
  35. Narita Y, Taguchi H, Nakamura T, Ueda A et al (2004) Characterization of the salt-inducible methionine synthase from barley leaves. Plant Sci 167:1009–1016CrossRefGoogle Scholar
  36. 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 5:4185–4196PubMedCrossRefGoogle Scholar
  37. 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 19:4061–4076PubMedCrossRefGoogle Scholar
  38. 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 70:277–283Google Scholar
  39. 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 60:438–446CrossRefGoogle Scholar
  40. Parry MAJ, Andralojc PJ, Khan S, Lea PJ, Keys AJ (2002) Rubisco activity: effects of drought stress. Ann Bot 89:833–839PubMedCrossRefGoogle Scholar
  41. Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle. Plant J 50:381–390PubMedCrossRefGoogle Scholar
  42. Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582PubMedCrossRefGoogle Scholar
  43. 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 203:173–179PubMedCrossRefGoogle Scholar
  44. 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 3:106–113Google Scholar
  45. 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 29:131–151PubMedCrossRefGoogle Scholar
  46. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858PubMedCrossRefGoogle Scholar
  47. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227PubMedCrossRefGoogle Scholar
  48. Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164PubMedCrossRefGoogle Scholar
  49. Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260PubMedCrossRefGoogle Scholar
  50. 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 229:955–964PubMedCrossRefGoogle Scholar
  51. 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 977–980Google Scholar
  52. 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 72–115Google Scholar
  53. Swami AK, Alam SI, Sengupta N, Sarin R (2011) Differential proteomic analysis of salt stress response in Sorghum bicolor leaves. Environ Exp Bot 71:321–328CrossRefGoogle Scholar
  54. 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 58:229–240PubMedCrossRefGoogle Scholar
  55. 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 62:641–652PubMedCrossRefGoogle Scholar
  56. Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917CrossRefGoogle Scholar
  57. Ting JP, Willingham SB, Bergstralh DT (2008) NLRs at the intersection of cell death and immunity. Nat Rev Immunol 8:372–379PubMedCrossRefGoogle Scholar
  58. 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 8:387–405PubMedCrossRefGoogle Scholar
  59. Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138PubMedCrossRefGoogle Scholar
  60. 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 55:2213–2218PubMedCrossRefGoogle Scholar
  61. 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 61:124–136CrossRefGoogle Scholar
  62. 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 9:244–252PubMedCrossRefGoogle Scholar
  63. 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 167:1477–1485PubMedCrossRefGoogle Scholar
  64. Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244PubMedCrossRefGoogle Scholar
  65. 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 49:226–241PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Ahmed Ashoub
    • 1
    • 2
    • 4
  • Tobias Beckhaus
    • 3
  • Thomas Berberich
    • 1
  • Michael Karas
    • 3
  • Wolfgang Brüggemann
    • 1
    • 4
  1. 1.Biodiversity and Climate Research Centre (BiK-F)Frankfurt am MainGermany
  2. 2.Agricultural Genetic Engineering Research Institute (AGERI)ARCGizaEgypt
  3. 3.Institute of Pharmaceutical ChemistryJohann Wolfgang Goethe-University FrankfurtFrankfurt am MainGermany
  4. 4.Institute of Ecology, Evolution, and DiversityJohann Wolfgang Goethe-University FrankfurtFrankfurt am MainGermany

Personalised recommendations