Skip to main content
Log in

Genome-Wide Identification and Expression Analysis of BES1 Family in Catharanthus roseus

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

Abstract

BES1 family genes function as the key regulator in BR signaling in various plant growth and development processes. As an intensively studied resource of vinblastine, a medicinal substance with anticancer properties, C. roseus is poorly understood in terms of the BES1 family and requires a comprehensive genomic and expressional analysis. In this study, seven CrBES1 family members were identified and classified into five groups based on the conserved motif, Pfam domain, gene structure, and phylogenetic analysis. Synteny of periwinkle and six other common species (tomato, Arabidopsis, pepper, rice, soybean, maize, and potato) were further analyzed to provide an insight into evolutionary relationships. Meanwhile, most cis-elements related to hormone, stress, and plant development were observed in the promoters of CrBES1 family genes. Subcellular localization showed five members located both in the nucleus and cytoplasm, implying the presence of dephosphorylated and phosphorylated form of these proteins, while another two members were located in the chloroplast. Furthermore, CrBES1-1, CrBES1-4, and CrBES1-7 principally expressed in flower, suggesting that they potentially function in flower development. Other members were observed to express in all organs. Moreover, CrBES1 genes exhibited variational expression in response to eight principal plant hormones. Notably, the expression level of CrBES1 genes presented a dominant downregulation in response to stress. This study reveals the genomic characterization of CrBES1 family through systematical analysis, as well as the functional features and expression patterns of their proteins, which lay a foundation for the functional research of CrBES1 family and flower development.

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

Similar content being viewed by others

References

  • Bai M-Y, Zhang L-Y, Gampala SS, Zhu S-W, Song W-Y, Chong K, Wang Z-Y (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci USA 104(34):13839–13844

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belkhadir Y, Jaillais Y (2015) The molecular circuitry of brassinosteroid signaling. New Phytol 206(2):522–540

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Khaliq A, Lu S, Xie M, Ma Z, Mao J, Chen B (2020) Genome-wide identification and characterization of the BES1 gene family in apple (Malus domestica). Plant Biol 22(4):723–733

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y (2017) Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in brassinosteroid-regulated plant growth and drought responses. Plant Cell 29(6):1425–1439. https://doi.org/10.1105/tpc.17.00364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L-G, Gao Z, Zhao Z, Liu X, Li Y, Zhang Y, Liu X, Sun Y, Tang W (2019a) BZR1 family transcription factors function redundantly and indispensably in BR signaling but exhibit BRI1-independent function in regulating anther development in Arabidopsis. Mol Plant 12(10):1408–1415

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Lv M, Wang Y, Wang P-A, Cui Y, Li M, Wang R, Gou X, Li J (2019b) BES1 is activated by EMS1-TPD1-SERK1/2-mediated signaling to control tapetum development in Arabidopsis thaliana. Nat Commun 10(1):4164

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: An Integrative Toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202

    Article  CAS  PubMed  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. https://doi.org/10.1146/annurev.arplant.49.1.427

    Article  CAS  PubMed  Google Scholar 

  • Eremina M, Unterholzner SJ, Rathnayake AI, Castellanos M, Khan M, Kugler KG, May ST, Mayer KFX, Rozhon W, Poppenberger B (2016) Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proc Natl Acad Sci USA 113(40):E5982–E5991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He J-X, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang Z-Y (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science (New York, NY) 307(5715):1634–1638

    Article  CAS  Google Scholar 

  • Jiang J, Zhang C, Wang X (2015) A recently evolved isoform of the transcription factor BES1 promotes brassinosteroid signaling and development in Arabidopsis thaliana. Plant Cell 27(2):361–374. https://doi.org/10.1105/tpc.114.133678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Sun Y, Burlingame AL, Wang ZY (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11(10):1254–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X (2011) A transient expression assay using arabidopsis mesophyll protoplasts. Bio-Protoc 1(10):e70

    Article  Google Scholar 

  • Li J, Li C (2019) Seventy-year major research progress in plant hormones byChinese scholars. Sci Sin Vitae 49(10):1227–1281

    Google Scholar 

  • Li L, Ye H, Guo H, Yin Y (2010) Arabidopsis IWS1 interacts with transcription factor BES1 and is involved in plant steroid hormone brassinosteroid regulated gene expression. Proc Natl Acad Sci USA 107(8):3918–3923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q-F, Wang C, Jiang L, Li S, Sun SSM, He J-X (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and Gibberellins in Arabidopsis. Sci Signal 5(244):72

    Article  Google Scholar 

  • Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S (2017) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10(4):545–559

    Article  CAS  PubMed  Google Scholar 

  • Li Q-F, Lu J, Yu J-W, Zhang C-Q, He J-X, Liu Q-Q (2018) The brassinosteroid-regulated transcription factors BZR1/BES1 function as a coordinator in multisignal-regulated plant growth. Biochim Biophys Acta 861(6):561–571

    Article  Google Scholar 

  • Li Y, He L, Li J, Chen J, Liu C (2018b) Genome-wide identification, characterization, and expression profiling of the legume BZR transcription factor gene family. Front Plant Sci 9:1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Li Q, Guo L, Wang H, Zhang Y, Fan C, Shen Y (2019) In silico genome-wide identification and comprehensive characterization of the BES1 gene family in soybean. Heliyon 5(6):e01868

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang T, Shi C, Peng Y, Tan H, Xin P, Yang Y, Wang F, Li X, Chu J, Huang J, Yin Y, Liu H (2020) Brassinosteroid-activated BRI1-EMS-SUPPRESSOR 1 inhibits flavonoid biosynthesis and coordinates growth and UV-B stress responses in plants. Plant Cell 32(10):3224–3239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Qanmber G, Lu L, Qin W, Liu J, Li J, Ma S, Yang Z, Yang Z (2018) Genome-wide analysis of BES1 genes in Gossypium revealed their evolutionary conserved roles in brassinosteroid signaling. Sci China Life Sci 61(12):1566–1582

    Article  CAS  PubMed  Google Scholar 

  • Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Li C, Ding Z (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14(1):e1007144

    Article  PubMed  PubMed Central  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(3):423–436

    Article  CAS  Google Scholar 

  • Nolan T, Chen J, Yin Y (2017) Cross-talk of Brassinosteroid signaling in controlling growth and stress responses. Biochem J 474(16):2641–2661

    Article  CAS  PubMed  Google Scholar 

  • Oh E, Zhu J-Y, Wang Z-Y (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14(8):802–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh E, Zhu J-Y, Bai M-Y, Arenhart RA, Sun Y, Wang Z-Y (2014) Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 3:e03031

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng P, Yan Z, Zhu Y, Li J (2008) Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation. Mol Plant 1(2):338–346

    Article  CAS  PubMed  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(4):1391–1403. https://doi.org/10.1105/tpc.110.081950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Saito M, Kondo Y, Fukuda H (2018) BES1 and BZR1 redundantly promote phloem and xylem differentiation. Plant Cell Physiol 59(3):590–600

    Article  CAS  PubMed  Google Scholar 

  • Shahnejat-Bushehri S, Tarkowska D, Sakuraba Y, Balazadeh S (2016) Arabidopsis NAC transcription factor JUB1 regulates GA/BR metabolism and signalling. Nat Plants 2:16013

    Article  CAS  PubMed  Google Scholar 

  • Song X-J (2017) Crop seed size: BR matters. Mol Plant 10(5):668–669

    Article  CAS  PubMed  Google Scholar 

  • Song X, Ma X, Li C, Hu J, Yang Q, Wang T, Wang L, Wang J, Guo D, Ge W, Wang Z, Li M, Wang Q, Ren T, Feng S, Wang L, Zhang W, Wang X (2018) Comprehensive analyses of the BES1 gene family in Brassica napus and examination of their evolutionary pattern in representative species. BMC Genom 19(1):346

    Article  Google Scholar 

  • Sreeramulu S, Mostizky Y, Sunitha S, Shani E, Nahum H, Salomon D, Hayun LB, Gruetter C, Rauh D, Ori N, Sessa G (2013) BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant J 74(6):905–919

    Article  CAS  PubMed  Google Scholar 

  • Su D, Xiang W, Wen L, Lu W, Shi Y, Liu Y, Li Z (2021) Genome-wide identification, characterization and expression analysis of BES1 gene family in tomato. BMC Plant Biol 21(1):161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Unterholzner SJ, Rozhon W, Papacek M, Ciomas J, Lange T, Kugler KG, Mayer KF, Sieberer T, Poppenberger B (2015) Brassinosteroids are master regulators of gibberellin biosynthesis in Arabidopsis. Plant Cell 27(8):2261–2272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Chory J (2006) Brassinosteroids regulate dissociation of BKI1, a negative regulator of BRI1 signaling, from the plasma membrane. Science 313(5790):1118–1122

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008) Sequential transphosphorylation of the BRI1/BAK1 receptor kinase complex impacts early events in brassinosteroid signaling. Dev Cell 15(2):220–235

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27(6):681–688

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Gao Y, Liu Y, Zhang X, Gu X, Ma D, Zhao Z, Yuan Z, Xue H, Liu H (2019) BES1-regulated BEE1 controls photoperiodic flowering downstream of blue light signaling pathway in Arabidopsis. New Phytol 223(3):1407–1419

    Article  CAS  PubMed  Google Scholar 

  • Wu P, Song X, Wang Z, Duan W, Hu R, Wang W, Li Y, Hou X (2016) Genome-wide analysis of the BES1 transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis). Plant Growth Regul 80(3):291–301

    Article  CAS  Google Scholar 

  • Xu G, Guo C, Shan H, Kong H (2012) Divergence of duplicate genes in exon–intron structure. Proc Natl Acad Sci USA 109(4):1187–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang X, Bai Y, Shang J, Xin R, Tang W (2016) The antagonistic regulation of abscisic acid-inhibited root growth by brassinosteroids is partially mediated via direct suppression of ABSCISIC ACID INSENSITIVE 5 expression by BRASSINAZOLE RESISTANT 1. Plant Cell Environ 39(9):1994–2003

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Wang Z-Y, 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(2):181–191

    Article  CAS  PubMed  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(2):249–259

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65(4):634–646

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Feng W, Sun F, Zhang Y, Qu J, Liu B, Lu F, Yang L, Fu F, Li W (2018) Cloning and characterization of BES1/BZR1 transcription factor genes in maize. Plant Growth Regul 86(2):235–249

    Article  CAS  Google Scholar 

  • Zhao X, Dou L, Gong Z, Wang X, Mao T (2019) BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol 221(2):908–918

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Jiao D, Zhang J, Xue C, Chen M, Yang Q (2020) Genome-wide identification and analysis of BES1/BZR1 transcription factor family in potato (Solanum tuberosum. L). Plant Growth Regul 92(2):375–387

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by National Natural Science Foundation of China (31400337)

Author information

Authors and Affiliations

Authors

Contributions

XD and ZHT conceived and designed the experiments. LZ and LP performed the experiments and validated the data. XD and ZX participated in original draft preparation. ZT and ZX supervised the research.

Corresponding author

Correspondence to Zhonghua Tang.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Handling Editor: Andrzej Bajguz.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 611 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, X., Pan, L. & Tang, Z. Genome-Wide Identification and Expression Analysis of BES1 Family in Catharanthus roseus. J Plant Growth Regul 42, 3851–3867 (2023). https://doi.org/10.1007/s00344-022-10849-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10849-1

Keywords

Navigation