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Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses

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Abstract

In addition to an essential role in plant development, brassinosteroids (BRs) appear to have the ability to protect plants against various environmental stresses. However, studies confirming the ability of BRs to modulate plant responses to different environmental stresses are lacking. Earlier we had demonstrated that treatment with 24-epibrassinolide (EBR), a BR, increases the basic thermotolerance of Brassica napus and tomato seedlings [Plant Mol Biol 40:333–342, 1999]. Here we demonstrate that EBR treatment enhances seedling tolerance to drought and cold stresses in both Arabidopsis thaliana and B. napus, and helps to overcome a salt-stress-induced inhibition of seed germination. The ability of EBR to confer tolerance in plants to a variety of stresses was confirmed through analysis of expression of a subset of drought and cold stress marker genes. Transcriptional changes in these genes were more apparent in EBR-treated A. thaliana, in particular during earlier time points of stress. To see if BR is essential for the heat stress (HS) response, we made use of BR-deficient mutants. Both det2-1 and dwf4 mutants still expressed heat shock proteins (hsps) to high levels during HS, indicating that although BR augments thermotolerance in plants, it is not necessary for hsp expression during HS.

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Abbreviations

BR:

Brassinosteroid

DRE:

Drought-responsive element

EBR:

24-Epibrassinolide

Hsp:

Heat shock protein

HS:

Heat stress

References

  • Anuradha S, Rao SSR (2001) Effect of brassinosteroids on salinity stress induced inhibition of seed germination and seedling growth of rice (Oryza sativa L.). Plant Growth Regul 33:151–153

    Article  CAS  Google Scholar 

  • Boothe JG, De Beus MD, Johnson-Flanagan AM (1995) Expression of a low-temperature-induced protein in Brassica napus. Plant Physiol 108:795–803

    PubMed  CAS  Google Scholar 

  • Clouse SD (2002) Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. Mol Cell 10:973–982

    Article  PubMed  CAS  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451

    Article  PubMed  CAS  Google Scholar 

  • Dhaubhadel S, Chaudhary S, Dobinson KF, Krishna P (1999) Treatment with 24-epibrassinolide, a brassinosteroid, increases the basic thermotolerance of Brassica napus and tomato seedlings. Plant Mol Biol 40:333–342

    Article  PubMed  CAS  Google Scholar 

  • Dhaubhadel S, Browning KS, Gallie DR, Krishna P (2002) Brassinosteroid functions to protect the translational machinery and heat-shock protein synthesis following thermal stress. Plant J 29:681–691

    Article  PubMed  CAS  Google Scholar 

  • Downing WL, Mauxion F, Fauvarque MO, Reviron MP, de Vienne D, Vartanian N, Giraudat J (1992) A Brassica napus transcript encoding a protein related to the Kunitz protease inhibitor family accumulates upon water stress in leaves, not in seeds. Plant J 2:685–693

    Article  PubMed  CAS  Google Scholar 

  • Gao YP, Young L, Bonham-Smith P, Gusta LV (1999) Characterization and expression of plasma and tonoplast membrane aquaporins in primed seed of Brassica napus during germination under stress conditions. Plant Mol Biol 40:635–644

    Article  PubMed  CAS  Google Scholar 

  • Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21

    Article  PubMed  CAS  Google Scholar 

  • Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  PubMed  CAS  Google Scholar 

  • Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    CAS  Google Scholar 

  • He RY, Wang GJ, Wang XS (1991) Effects of brassinolide on growth and chilling resistance of maize seedlings. In: Cutler HG, Yokota T, Adam G (eds) Brassinosteroids: chemistry, bioactivity and applications. American Chemical Society Symposium Series 474. American Chemical Society, Washington pp 220–230

    Google Scholar 

  • Iwasaki T, Yamaguchi-Shinozaki K, Shinozaki K (1995) Identification of a cis-regulatory region of a gene in Arabidopsis thaliana whose induction by dehydration is mediated by abscisic acid and requires protein synthesis. Mol Gen Genet 247:391–398

    Article  PubMed  CAS  Google Scholar 

  • Katsumi M (1991) Physiological modes of brassinolide action in cucumber hypocotyl growth. In: Cutler HG, Yokota T, Adam G (eds) Brassinosteroids: chemistry, bioactivity and applications. American Chemical Society Symposium Series 474. American Chemical Society, Washington, pp. 246–254

    Google Scholar 

  • Khripach V, Zhabinskii V, de Groot A (2000) Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for the XXI century. Ann Bot 86:441–447

    Article  CAS  Google Scholar 

  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K (1994) Characterization of two cDNAs (ERD10 and ERD14) corresponding to genes that respond rapidly to dehydration stress in Arabidopsis thaliana. Plant Cell Physiol 35:225–231

    PubMed  CAS  Google Scholar 

  • Ko K, Bornemisza O, Kourtz ZW, Plaxton WC, Cashmore AR (1992) Isolation and characterization of a cDNA clone encoding a cognate 70 kDa heat shock protein of the chloroplast envelope. J Biol Chem 267:2986–2993

    PubMed  CAS  Google Scholar 

  • Krishna P (2003a) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297

    Article  CAS  Google Scholar 

  • Krishna P (2003b) Plant responses to heat stress. Top Curr Genet 4:73–101

    Google Scholar 

  • Krishna P, Sacco M, Cherutti JF, Hill S (1995) Cold induced accumulation of hsp90 transcripts in Brassica napus. Plant Physiol 107:915–923

    PubMed  CAS  Google Scholar 

  • Krishna P, Reddy RK, Sacco M, Frappier JR, Felsheim RF (1997) Analysis of the native forms of the 90 kDa heat shock protein (hsp90) in plant cytosolic extracts. Plant Mol Biol 33:457–466

    Article  PubMed  CAS  Google Scholar 

  • Kulaeva ON, Burkhanova EA, Fedina AB, Khokhlova VA, Bokebayeva GA, Vorbrodt HM, Adam G (1991) Effect of brassinosteroids on protein synthesis and plant-cell ultrastructure under stress conditions. In: Cutler HG, Yokota T, Adam G (eds) Brassinosteroids: chemistry, bioactivity and applications. American Chemical Society Symposium Series 474. American Chemical Society, Washington, pp 141–155

    Google Scholar 

  • Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • Mandava NB (1988) Plant growth-promoting brassinosteroids. Annu Rev Plant Physiol Plant Mol Biol 39:23–52

    Article  CAS  Google Scholar 

  • Morillon R, Catterou M, Sangwan RS, Sangwan BS, Lassalles JP (2001) Brassinolide may control aquaporin activities in Arabidopsis thaliana. Planta 212:199–204

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Mussig C, Altmann T (2003) Genomic brassinosteroid effects. J Plant Growth Regul 22:313–324

    Article  PubMed  Google Scholar 

  • Mussig C, Fischer S, Altmann T (2002) Brassinosteroid-regulated gene expression. Plant Physiol 129:1241–1251

    Article  PubMed  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 

  • Sairam RK (1994) Effects of homobrassinolide application on plant metabolism and grain yield under irrigated and moisture-stress conditions of two wheat varieties. Plant Growth Regul 14:173–181

    Article  CAS  Google Scholar 

  • Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288

    Article  PubMed  CAS  Google Scholar 

  • Sasse JM, Smith R, Hudson I (1995) Effect of 24-epibrassinolide on germination of seeds of Eucalyptus camaldulensis in saline conditions. Proc Plant Growth Regul Soc Am 22:136–141

    Google Scholar 

  • Schirmer EC, Lindquist S, Vierling E (1994) An Arabidopsis heat shock protein complements a thermotolerance defect in yeast. Plant Cell 6:1899–1909

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (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

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Stroeher VL, Boothe JG, Good AG (1995) Molecular cloning and expression of a turgor-responsive gene in Brassica napus. Plant Mol Biol 27:541–551

    Article  PubMed  CAS  Google Scholar 

  • Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altmann T, Redei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1993) Genes induced during cold acclimation in higher plants. In: Steponkus PL (eds) Advances in low-temperature biology, vol. 2. JAI, London, pp 183–210

    Google Scholar 

  • Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signaling. Nature 441:96–100

    Article  PubMed  CAS  Google Scholar 

  • Vert G, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Wang Q, Chong K, Wang F, Wang L, Bai M, Jia C (2006) The brassinosteroid signal transduction pathway. Cell Res 16:427–434

    Article  PubMed  CAS  Google Scholar 

  • Weretilnyk E, Orr W, White TC, Iu B, Singh J (1993) Characterization of three related low-temperature-regulated cDNAs from winter Brassica napus. Plant Physiol 101:171–177

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Natural Sciences and Engineering Research Council of Canada and CIDtech Inc. We thank Drs J. Li and E. Vierling for providing det2-1 mutant seeds and anti-hsp101 antibody, respectively, and Debbie Dong for excellent technical help.

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Authors and Affiliations

  1. Department of Biology, The University of Western Ontario, London, ON, Canada, N6A 5B7

    Sateesh Kagale, Uday K. Divi & Priti Krishna

  2. Plant Biotechnology Institute, National Research Council of Canada, 110 Gymnasium Place, Saskatoon, SK, Canada, S7N 0W9

    Joan E. Krochko & Wilfred A. Keller

Authors
  1. Sateesh Kagale
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  2. Uday K. Divi
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  3. Joan E. Krochko
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  4. Wilfred A. Keller
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  5. Priti Krishna
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Correspondence to Priti Krishna.

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Kagale, S., Divi, U.K., Krochko, J.E. et al. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225, 353–364 (2007). https://doi.org/10.1007/s00425-006-0361-6

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  • DOI: https://doi.org/10.1007/s00425-006-0361-6

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