Skip to main content
Log in

Characterization of Small Heat Shock Proteins Associated with Maize Tolerance to Combined Drought and Heat Stress

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

To investigate how the mechanisms of small heat shock proteins (sHSPs) in regulating maize leaves respond to the combination of drought and heat stress, leaf protein patterns were monitored using a proteomic approach in maize plants exposed to combined drought and heat stress. Two-dimensional electrophoresis (2-DE) was used to identify combined drought- and heat-responsive protein spots in maize leaves. After Coomassie brilliant blue staining, approximately 450 protein spots were reproducibly detected on each gel, wherein 7 protein spots were expressed only under heat and combined drought and heat stress but were almost undetected under control and drought. Using MALDI-TOF mass spectrometry, a total of seven proteins were identified, including cytochrome b6-f complex iron-sulfur subunit, sHSP17.4, sHSP17.2, sHSP26, guanine nucleotide-binding protein β-subunit-like protein, putative uncharacterized protein, and granule-bound starch synthase IIa. Moreover, the gene expression of three sHSPs was analyzed at the transcriptional level and indicated that all three sHSPs were expressed under several treatments although their expression levels were obviously more enhanced by heat and combined drought and heat stress than by control and drought. In investigations of the effect of abscisic acid (ABA) on the three sHSPs, pretreatment with 100 μM ABA enhanced substantially the expression of the three sHSPs at the protein level, but only slightly at the mRNA level. These results show that transcription levels are not completely concomitant with translation and suggest that ABA induces the post-transcriptional regulation of sHSP17.2, sHSP17.4, and sHSP26 expression, which can lead to a better understanding of the mechanisms of plant response to the combination of drought and heat stress.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CBB:

Coomassie brilliant blue

cAPX:

Cytosolic ascorbate peroxidase

DTT:

Dithiothreitol

IEF:

Isoelectric focusing

MALDI-TOF:

Matrix-assisted laser desorption/ionization time of flight

MS:

Mass spectrometry

PMSF:

Phenylmethanesulfonyl fluoride

PVP:

Polyvinylpyrrolidone

PVPP:

Polyvinylpolypyrrolidone

pI:

Isoelectric point

sHSPs:

Small heat shock protein

T:

Tungstate

2-DE:

Two-dimensional electrophoresis

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

TCA:

Trichloroacetic acid

TFA:

Trifluoroacetic acid

References

  • Agrawal GK, Rakwal R (2006) Rice proteomics: a cornerstone for cereal food crop proteomes. Mass Spectrom Rev 25:1–53

    Article  CAS  PubMed  Google Scholar 

  • Ahn YJ, Zimmerman JL (2006) Introduction of the carrot HSP17.7 into potato (Solanum tuberosum L.) enhances cellular membrane stability and tuberization in vitro. Plant Cell Environ 29:95–104

    Article  CAS  PubMed  Google Scholar 

  • Almoguera C, Jordano J (1994) Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs. Biotechnol Appl Biochem 19:41–49

    Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, MD, pp 1158–1249

    Google Scholar 

  • Charng YY, Liu HC, Liu NY, Hsu FC, Ko SS (2006) Arabidopsis Hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140:1297–1305

    Article  CAS  PubMed  Google Scholar 

  • Colmenero-Flores JM, Campos F, Garciarrubio A, Covarrubias AA (1997) Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Mol Biol 35:393–405

    Article  CAS  PubMed  Google Scholar 

  • Dong JZ, Dunstan DI (1996) Characterization of three heat-shock-protein genes and their developmental regulation during somatic embryogenesis in white spruce [Picea glauca (Moench) Voss]. Planta 200:85–91

    Article  CAS  PubMed  Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908

    Article  CAS  PubMed  Google Scholar 

  • Gong M, Li YJ, Chen SZ (1998) Abscisic acid induced thermotolerance in maize seedlings is mediated by Ca2+ and associated with antioxidant systems. J Plant Physiol 153:488–496

    CAS  Google Scholar 

  • Guo SJ, Zhou HY, Zhang XS, Li XG, Meng QW (2007) Overexpression of CaHSP26 in transgenic tobacco alleviates photoinhibition of PSII and PSI during chilling stress under low irradiance. J Plant Physiol 164:126–136

    Article  CAS  PubMed  Google Scholar 

  • Hansen H, Grossmann K (2000) Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiol 124:1437–1448

    Article  CAS  PubMed  Google Scholar 

  • Hu XL, Jiang MY, Zhang JH, Tan MP, Zhang AY (2008) Cross-talk between Ca2+/CaM and H2O2 in abscisic acid-induced antioxidant defense in leaves of maize plants exposed to water stress. Plant Growth Regul 55:183–198

    Article  Google Scholar 

  • Hu XL, Liu RX, Li YH, Wang W, Tai FJ, Li CH (2010) Heat shock protein 70 regulates the abscisic acid–induced antioxidant response of maize to combined drought and heat stress. Plant Growth Regul 60(3):225–235

    Article  CAS  Google Scholar 

  • Huang B, Xu CP (2008) Identification and characterization of proteins associated with plant tolerance to heat stress. J Integr Plant Biol 50:1230–1237

    Article  CAS  PubMed  Google Scholar 

  • Jaya N, Garcia V, Vierling E (2009) Substrate binding site flexibility of the small heat shock protein molecular chaperones. Proc Natl Acad Sci USA 106:15604–15609

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen JA, Nguyen HT (2004) Isolation, sequence and expression of a cDNA encoding a Class I heat shock protein (HSP17.2) in maize. Plant Sci 97:169–175

    Article  Google Scholar 

  • Lee BH, Tanaka Y, Iwasaki T, Yamamoto N, Kayano T, Miyao M (1998) Evolutionary origin of two genes for chloroplast small heat shock protein of tobacco. Plant Mol Biol 37:1035–1043

    Article  CAS  PubMed  Google Scholar 

  • Lee BH, Won SH, Lee HS, Miyao M, Chung Kim WJ, Jo J (2000) Expression of the chloroplast-localized small heat shock protein by oxidative stress in rice. Gene 245:283–290

    Article  CAS  PubMed  Google Scholar 

  • Lee DG, Ahsan N, Lee SH, Kang KY, Bahk JD, Lee IJ, Lee BH (2007) A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 7:3369–3383

    Article  CAS  PubMed  Google Scholar 

  • Low D, Brandle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211:575–582

    Article  CAS  PubMed  Google Scholar 

  • Maqbool A, Zahur M, Irfan M, Qaiser U, Rashid B, Husnain T, Riazuddin S (2007) Identification, characterization and expression of drought related alpha-crystalline heat shock protein gene (GHSP26) from Desi Cotton. Crop Sci 47:2437–2444

    Article  CAS  Google Scholar 

  • Neta-Sharir I, Tal Isaacson T, Lurie S, Weissa D (2005) Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838

    Article  CAS  PubMed  Google Scholar 

  • Osteryoung KW, Vierling E (1994) Dynamics of small heat shock protein distribution within the chloroplasts of higher plants. J Biol Chem 269:28676–28682

    CAS  PubMed  Google Scholar 

  • Papdi C, Ábrahám E, Joseph PM, Cristina Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147:528–542

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  CAS  PubMed  Google Scholar 

  • Sanmiya K, Suzuki K, Egawa Y, Shono M (2004) Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants. FEBS Lett 557:265–268

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep 27:329–334

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Bernard C, van de Cotte B, Montagu MV, Verbruggen N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    CAS  PubMed  Google Scholar 

  • Thomson AM, Brown RA, Rosenberg NJ, Izaurralde RC, Benson V (2005) Climate change impacts for the conterminous USA: an integrated assessment. Part 3. Dryland production of grain and forage crops. Clim Change 69:43–65

    Article  CAS  Google Scholar 

  • Vierling E (1991) The role of heat shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 42:579–620

    Article  CAS  Google Scholar 

  • Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61:733–746

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, 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  CAS  PubMed  Google Scholar 

  • Wang W, Vignani R, Scali M, Cresti M (2006) A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27:2782–2786

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Bianchi L, Scali M, Liu LW, Bini L, Cresti M (2009) Proteomic analysis of β-1, 3-glucanase in grape berry tissues. Acta Physiol Plant 31:597–604

    Article  CAS  Google Scholar 

  • Yang KZ, Xia C, Liu XL, Dou XY, Wang W, Chen LQ, Zhang XQ, Xie LF, He L, Ma X, Ye D (2009) A mutation in Thermosensitive Male Sterile 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophytic male sterility in Arabidopsis. Plant J 57:870–882

    Article  CAS  PubMed  Google Scholar 

  • Yi SY, Sun AQ, Sun Y, Yang JY, Chun-Mei Zhao, Liu J (2006) Differential regulation of Lehsp23.8 in tomato plants: analysis of a multiple stress-inducible promoter. Plant Sci 171:398–407

    Article  CAS  Google Scholar 

  • Yu JH, Kim KP, Park SM, Hong CB (2005) Biochemical analysis of a cytosolic small heat shock protein, NtHSP18.3, from Nicotiana tabacum. Mol Cells 19:328–333

    CAS  PubMed  Google Scholar 

  • Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, Zhang X (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166:851–861

    Article  CAS  PubMed  Google Scholar 

  • Zahur M, Maqbool A, Irfan M, Khan BMY, Qaiser U, Rashid B, Husnain T, Riazuddin S (2009) Functional analysis of cotton small heat shock protein promoter region in response to abiotic stresses in tobacco using Agrobacterium-mediated transient assay. Mol Biol Rep 36:1915–1921

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant No. 30800667 to X. L. Hu), the China Postdoctoral Science Foundation (grant Nos. 20080440824 and 200902357 to X. L. Hu), the Natural Science Foundation of Henan Educational Committee (grant No. 2008A180011 to X. L. Hu), the Foundation for University Key Teacher by the Ministry of Education (grant No. 2009GGJS-028 to X. L. Hu), and the Foundation of Henan Major Public Projects (grant No. 091100910100).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiuli Hu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hu, X., Li, Y., Li, C. et al. Characterization of Small Heat Shock Proteins Associated with Maize Tolerance to Combined Drought and Heat Stress. J Plant Growth Regul 29, 455–464 (2010). https://doi.org/10.1007/s00344-010-9157-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-010-9157-9

Keywords

Navigation