Skip to main content
Log in

Characterization of Brassinazole resistant (BZR) gene family and stress induced expression in Eucalyptus grandis

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Brassinosteroids (BRs) are a group of plant hormones which play a pivotal role in modulating cell elongation, stress responses, vascular differentiation and senescence. In response to BRs, BRASSINAZOLE-RESISTANT (BZR) transcription factors (TFs) accumulate in the nucleus, where they modulate thousands of target genes and coordinate many biological processes, especially in regulating defense against biotic and abiotic stresses. In this study, 6 BZR TFs of Eucalyptus grandis (EgrBZR) from a genome-wide survey were characterized by sequence analysis and expression profiling against several abiotic stresses. The results showed that BZR gene family in Eucalyptus was slightly smaller compared to Populus and Arabidopsis, but all phylogenetic groups were represented. Various systematic in silico analysis of these TFs validated the basic properties of BZRs, whereas comparative studies showed a high degree of similarity with recognized BZRs of other plant species. In the organ-specific expression analyses, 4 EgrBZRs were expressed in vascular tissue indicating their possible functions in wood formation. Meanwhile, almost all EgrBZR genes showed differential transcript abundance levels in response to exogenously applied BR, MeJA, and SA, and salt and cold stresses. Besides, protein interaction analysis showed that all EgrBZR genes were associated with BR signaling directly or indirectly. These TFs were proposed as transcriptional activators or repressors of abiotic stress response and growth and development pathways of E. grandis by participating in BR signaling processes. These findings would be helpful in resolving the regulatory mechanism of EgrBZRs in stress resistance conditions but require further functional study of these potential TFs in Eucalyptus.

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

Similar content being viewed by others

References

  • Baroja-Fernández E, Muñoz FJ, Li J, Bahaji A, Almagro G, Montero M, Etxeberria E, Hidalgo M, Sesma MT, Pozueta-Romero J (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci 109:321–326

    Article  PubMed  Google Scholar 

  • de Oliveira LA, Breton MC, Bastolla FM, Camargo SDS, Margis R, Frazzon J, Pasquali G (2011) Reference genes for the normalization of gene expression in Eucalyptus species. Plant Cell Physiol 53:405–422

    Article  PubMed  CAS  Google Scholar 

  • Guo R, Qian H, Shen W, Liu L, Zhang M, Cai C, Zhao Y, Qiao J, Wang Q (2013) BZR1 and BES1 participate in regulation of glucosinolate biosynthesis by brassinosteroids in Arabidopsis. J Exp Bot 64:2401–2412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang Z-Y (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307:1634–1638

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jennifer Lachowiec, G. A. M., Karla Schultz, Christine Queitsch. (2016). Redundancy, feedback, and robustness in the Arabidopsis thaliana BZR/BEH gene family. bioRxiv p 053447

  • Jin H, Do J, Shin SJ, Choi JW, Choi YI, Kim W, Kwon M (2014) Exogenously applied 24-epi brassinolide reduces lignification and alters cell wall carbohydrate biosynthesis in the secondary xylem of Liriodendron tulipifera. Phytochemistry 101:40–51

    Article  PubMed  CAS  Google Scholar 

  • Kim B, Fujioka S, Kwon M, Jeon J, Choe S (2013) Arabidopsis Brassinosteroid-overproducing gulliver3-D/dwarf4-D mutants exhibit altered responses to Jasmonic acid and pathogen. Plant Cell Rep 32:1139–1149

    Article  PubMed  CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li QF, He JX (2016) BZR1 interacts with HY5 to mediate brassinosteroid-and light-regulated cotyledon opening in Arabidopsis in darkness. Mol Plant 9:113–125

    Article  PubMed  CAS  Google Scholar 

  • Manoli A, Trevisan S, Quaggiotti S, Varotto S (2018) Identification and characterization of the BZR transcription factor family and its expression in response to abiotic stresses in Zea mays L. Plant Growth Regul 84:423–436

    Article  CAS  Google Scholar 

  • Mizrachi E, Hefer CA, Ranik M, Joubert F, Myburg AA (2010) De novo assembled expressed gene catalog of a fast-growing Eucalyptus tree produced by Illumina mRNA-Seq. BMC Genom 11:681

    Article  CAS  Google Scholar 

  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D (2014) The genome of Eucalyptus grandis. Nature 510:356–362

    Article  PubMed  CAS  Google Scholar 

  • Nasim M, Qureshi RH, Aziz T, Saqib M, Nawaz S, Sahi ST, Pervaiz S (2008) Growth and ionic composition of salt-stressed Eucalyptus camaldulensis and Eucalyptus tereticornis. Pak J Bot 40:799–805

    CAS  Google Scholar 

  • Oh E, Zhu JY, Wang ZY (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14:802–809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E et al (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    Article  PubMed  PubMed Central  Google Scholar 

  • Reinhold H, Soyk S, Šimková K, Hostettler C, Marafino J, Mainiero S, Vaughan CK, Monroe JD, Zeeman SC (2011) β-amylase–like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23:1391–1403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rosa Lozano-Durán APM, Boutrot Freddy, Segonzac Cécile, Somssich Imre E, Zipfel Cyril (2013) The transcriptional regulator BZR1 mediates trade-off between plant innate immunity and growth. eLIFE 2:e00983

    Article  PubMed  PubMed Central  Google Scholar 

  • Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Kang JG, Nou IS (2015) Molecular characterization of BZR transcription factor family and abiotic stress induced expression profiling in Brassica rapa. Plant Physiol Biochem 92:92–104

    Article  PubMed  CAS  Google Scholar 

  • Salazar-Henao JE, Lehner R, Betegón-Putze I, Vilarrasa-Blasi J, Caño-Delgado AI (2016) BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of the Arabidopsis primary root. J Exp Bot 67:4951–4961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seung D, Thalmann M, Sparla F, Abou Hachem M, Lee SK, Issakidis-Bourguet E, Svensson B, Zeeman SC, Santelia D (2013) Arabidopsis thaliana AMY3 Is a unique redox-regulated chloroplastic α-amylase. J Biol Chem 288:33620–33633

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Soyk S, Šimková K, Zürcher E, Luginbühl L, Brand LH, Vaughan CK, Wanke D, Zeeman SC (2014) The enzyme-like domain of Arabidopsis nuclear β-amylases is critical for DNA sequence recognition and transcriptional activation. Plant Cell 26:1746–1763

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E et al (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim T, Zhou H, Deng Z, Gampala SS et al (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13(2):124–131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tibbits WN, White TL, Hodge GR, Nmg B (2006) Genetic variation in frost resistance of Eucalyptus globulus ssp. globulus assessed by artificial freezing in winter. Aust J Bot 54:521–529

    Article  Google Scholar 

  • Verhoef N, Yokota T, Shibata K, de Boer G-J, Gerats T, Vandenbussche M, Koes R, Souer E (2013) Brassinosteroid biosynthesis and signalling in Petunia hybrida. J Exp Bot 64:2435–2448

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513

    Article  PubMed  CAS  Google Scholar 

  • Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant 9:86–100

    Article  PubMed  CAS  Google Scholar 

  • Yang CJ, Zhang C, Lu YN, Jin JQ, Wang XL (2011) The mechanisms of brassinosteroids’ action: from signal transduction to plant development. Mol Plant 4:588–600

    Article  PubMed  CAS  Google Scholar 

  • Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191

    Article  PubMed  CAS  Google Scholar 

  • Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P et al (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65:634–646

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Ye H, Guo H, Johnson A, Zhang M, Lin H, Yin Y (2013a) Transcription factor HAT1 is phosphorylated by bin2 kinase and mediates brassinsteroid repressed gene expression in Arabidopsis. Plant J 77:59–70

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Li B, Xu Y, Li H, Li S, Zhang D, Mao Z, Guo S, Yang C, Weng Y et al (2013b) The cyclophilin CYP20-2 modulates the conformation of BRASSINAZOLE-RESISTANT1, which binds the promoter of FLOWERING LOCUS D to regulate flowering in Arabidopsis. Plant Cell 25:2504–2521

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Zhang YJ, Yang BJ, Yu XX, Wang D, Zu SH, Xue HW, Lin WH (2016) Functional characterization of GmBZL2 (AtBZR1 like gene) reveals the conserved BR signaling regulation in Glycine max. Scientific Reports 6:31134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao J, Peng P, Schmitz RJ, Decker AD, Tax FE, Li J (2002) Two putative BIN2 substrates are nuclear components of brassinosteroid signaling. Plant Physiol 130:1221–1229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhu JY, Sae-Seaw J, Wang ZY (2013) Brassinosteroid signalling. Development 140:1615–1620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge National Natural Science Foundation of China (Grant Number: 31400554) and the Fundamental Research Funds for the Central Non-profit Research Institution of CAF (Grant Noumber: CAFYBB2014QB040).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bingshan Zeng.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, C., Guo, G., Yan, H. et al. Characterization of Brassinazole resistant (BZR) gene family and stress induced expression in Eucalyptus grandis. Physiol Mol Biol Plants 24, 821–831 (2018). https://doi.org/10.1007/s12298-018-0543-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-018-0543-2

Keywords

Navigation