Skip to main content
SpringerLink
Log in

Genome-wide identification and expression analysis of the bZIP gene family in silver birch (Betula pendula Roth.)

  • Original Paper
  • Published:
Journal of Forestry Research Aims and scope Submit manuscript

Abstract

Basic Leu zipper (bZIP) genes play pivotal, versatile roles in abiotic or biotic stress responses and in other biological processes. Knowledge on the evolutionary relationships and patterns of gene expression of bZIP family members in woody plants, however, has been limited. Here we identified and characterized 47 BpbZIP genes across the silver birch (Betula pendula Roth.) genome. With reference to bZIP classifications for Arabidopsis thaliana, all BpbZIP proteins clustered among 10 groups in phylogeny. The bZIP domains were divided into five patterns based on intron positions and splicing phases. A total of 24 conserved motifs were detected in BpbZIPs with high group specificity. We also analyzed the protein structure of the BpAREB/ABF/ABI5 subfamily, the most important subfamily in the bZIP family. Expression analyses demonstrated that BpbZIP genes were widely involved in abscisic acid, salt, drought, and heat stress responses, with BpbZIP07/ABF4 and BpbZIP21/ABF2 most highly expressed. Our results on genome-wide identification, evolutionary relationships, gene structure, and motif and promoter element identification for BpbZIP family members in silver birch provide a comprehensive understanding of bZIP transcription factors in birch and will lead to a deeper understanding of their evolution and potential biological functions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Balázs A, Pócsi I, Hamari Z, Leiter É, Emri T, Miskei M, Oláh J, Tóth V, Hegedűs N, Prade RA, Molnár M, Pócsi I (2010) AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. Mol Genet Genom 283:289–303

    Article  CAS  Google Scholar 

  • Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Chen W, Zhou JL, He H, Chen LB, Chen HD, Deng XW (2012) Basic leucine zipper transcription factor OsbZIP16 positively regulates drought resistance in rice. Plant Sci 193–194:8–17

    Article  PubMed  CAS  Google Scholar 

  • Chen S, Wang YC, Yu LL, Zheng T, Wang S, Yue Z, Jiang J, Kumari S, Zheng CF, Tang H, Li J, Li YQ, Chen JJ, Zhang WB, Kuang HH, Robertson JS, Zhao PX, Li HY, Shu SQ, Yordanov YS, Huang HJ, Goodstein DM, Gai Y, Qi Q, Min JM, Xu CY, Wang SB, Qu GZ, Paterson AH, Sankoff D, Wei HR, Liu GF, Yang CP (2021) Genome sequence and evolution of Betula platyphylla. Hortic Res 8:37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen S, Lin X, Zhang DW, Li Q, Zhao XY, Chen Su (2019) Genome-wide analysis of NAC gene family in Betula pendula. Forests 10:741

    Article  Google Scholar 

  • Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucl Acids Res 39:W29–W37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster R, Izawa T, Chua NH (1994) Plant bZIP proteins gather at ACGT elements. FASEB J 8:192–200

    Article  CAS  PubMed  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan YC, Ren HB, Xie H, Ma ZY, Chen F (2009) Identification and characterization of bZIP-type transcription factors involved in carrot (Daucus carota L.) somatic embryogenesis. Plant J 60:207–217

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucl Acids Res 35:w585–w587

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya TYC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473

    Article  CAS  PubMed  Google Scholar 

  • Hu B, Jin JP, Guo AY, Zhang H, Luo JC, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Izawa T, Foster R, Nakajima M, Shimamoto K, Chua NH (1994) The rice bZIP transcriptional activator RITA-1 is highly expressed during seed development. Plant Cell 6:1277–1287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Ji LX, Wang J, Ye MX, Li Y, Guo B, Chen Z, Li H, An XM (2013) Identification and characterization of the Populus AREB/ABF subfamily. J Integr Plant Biol 55:177–186

    Article  CAS  PubMed  Google Scholar 

  • Jin ZW, Xu W, Liu AZ (2014) Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta 239:299–312

    Article  CAS  PubMed  Google Scholar 

  • Kaminaka H, Näke C, Epple P, Dittgen J, Schütze K, Chaban C, Holt BF, Merkle T, Schäfer E, Harter K, Dangl JL (2006) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kouzarides T, Ziff E (1989) Leucine zippers of fos, jun and GCN4 dictate dimerization specificity and thereby control DNA binding. Nature 340:568–571

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Landschulz WH, Johnson PF, McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759–1764

    Article  CAS  PubMed  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer YV, 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. Nucl Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li DD, Xu XM, Hu XQ, Liu QG, Wang ZC, Zhang HZ, Wang H, Wei M, Wang HZ, Liu HM, Li CH (2015) Genome-wide analysis and heavy metal-induced expression profiling of the HMA gene family in Populus trichocarpa. Front Plant Sci 6:1149

    PubMed  PubMed Central  Google Scholar 

  • Liu CY, Xu HW, Han R, Wang S, Liu GF, Chen S, Chen JY, Bian XY, Jiang J (2019a) Overexpression of BpCUC2 influences leaf shape and internode development in Betula pendula. Int J Mol Sci 20:4722

    Article  CAS  PubMed Central  Google Scholar 

  • Liu JY, Chen NN, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng ZMM (2014) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genom 15:281

    Article  CAS  Google Scholar 

  • Liu TF, Zhou TT, Lian MT, Liu TT, Hou J, Ijaz R, Song BT (2019b) Genome-wide identification and characterization of the AREB/ABF/ABI5 subfamily members from Solanum tuberosum. Int J Mol Sci 20:311

    Article  PubMed Central  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishizawa-Yokoi A, Yoshida E, Yabuta Y, Shigeoka S (2009) Analysis of the regulation of target genes by an Arabidopsis heat shock transcription factor, HsfA2. Biosci Biotechnol Biochem 73:890–895

    Article  CAS  PubMed  Google Scholar 

  • Salojärvi J, Smolander OP, Nieminen K, Rajaraman S, Safronov O, Safdari P, Lamminmäki A, Immanen J, Lan T, Tanskanen J, Rastas P, Amiryousefi A, Jayaprakash B, Kammonen JI, Hagqvist R, Eswaran G, Ahonen VH, Serra JA, Asiegbu FO, De Dios Barajas-Lopez J, Blande D, Blokhina O, Blomster T, Broholm S, Brosché M, Cui FQ, Dardick C, Ehonen SE, Elomaa P, Escamez S, Fagerstedt KV, Fujii H, Gauthier A, Gollan PJ, Halimaa P, Heino PI, Himanen K, Hollender C, Kangasjärvi S, Kauppinen L, Kelleher CT, Kontunen-Soppela S, Koskinen JP, Kovalchuk A, Kärenlampi SO, Kärkönen AK, Lim KJ, Leppälä J, Macpherson L, Mikola J, Mouhu K, Mähönen AP, Niinemets Ü, Oksanen E, Overmyer K, Palva ET, Pazouki L, Pennanen V, Puhakainen T, Poczai P, Possen BJHM, Punkkinen M, Rahikainen MM, Rousi M, Ruonala R, van der Schoot C, Shapiguzov A, Sierla M, Sipilä TP, Sutela S, Teeri TH, Tervahauta AI, Vaattovaara A, Vahala J, Vetchinnikova L, Welling A, Wrzaczek M, Xu EJ, Paulin LG, Schulman AH, Lascoux M, Albert VA, Auvinen P, Helariutta Y, Kangasjärvi J (2017) Genome sequencing and population genomic analyses provide insights into the adaptive landscape of silver birch. Nat Genet 49:904–912

    Article  PubMed  CAS  Google Scholar 

  • Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shiota H, Ko S, Wada S, Otsu CT, Tanaka I, Kamada H (2008) A carrot G-box binding factor-type basic region/leucine zipper factor DcBZ1 is involved in abscisic acid signal transduction in somatic embryogenesis. Plant Physiol Biochem 46:550–558

    Article  CAS  PubMed  Google Scholar 

  • Storozhenko S, De Pauw P, Van Montagu M, Inzé D, Kushnir S (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol 118:1005–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strathmann A, Kuhlmann M, Heinekamp T, Dröge-Laser W (2001) BZI-1 specifically heterodimerises with the tobacco bZIP transcription factors BZI-2, BZI-3/TBZF and BZI-4, and is functionally involved in flower development. Plant J 28:397–408

    Article  CAS  PubMed  Google Scholar 

  • Sun MY, Fu XL, Tan QP, Liu L, Chen M, Zhu CY, Li L, Chen XD, Gao DS (2016) Analysis of basic leucine zipper genes and their expression during bud dormancy in peach (Prunus persica). Plant Physiol Biochem 104:54–70

    Article  CAS  PubMed  Google Scholar 

  • Sun XC, Hu CX, Tan QL, Liu JS, Liu HG (2009) Effects of molybdenum on expression of cold-responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-temperature stress. Ann Bot 104:345–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki M, Ketterling MG, Li QB, McCarty DR (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132:1664–1677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Bassil E, Hamilton JS, Inupakutika MA, Zandalinas SI, Tripathy D, Luo Y, Dion E, Fukui G, Kumazaki A, Nakano R, Rivero RM, Verbeck GF, Azad RK, Blumwald E, Mittler R (2016) ABA is required for plant acclimation to a combination of salt and heat stress. PLoS ONE 11:e0147625

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2007) The Arabidopsis information resource (TAIR): gene structure and function annotation. Nucl Acids Res 36:D1009–D1014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang N, Zhang H, Li XH, Xiao JH, Xiong LZ (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tippmann HF (2004) Analysis for free: comparing programs for sequence analysis. Brief Bioinform 5:82–87

    Article  CAS  PubMed  Google Scholar 

  • Toh S, McCourt P, Tsuchiya Y (2012) HY5 is involved in strigolactone-dependent seed germination in Arabidopsis. Plant Signal Behav 7:556–558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulm R, Baumann A, Oravecz A, Máté Z, Adám É, Oakeley EJ, Schäfer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. Proc Natl Acad Sci USA 101:1397–1402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vinson CR, Sigler PB, McKnight SL (1989) Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science 246:911–916

    Article  CAS  PubMed  Google Scholar 

  • Wang JZ, Zhou JX, Zhang BL, Vanitha J, Ramachandran S, Jiang SY (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53:212–231

    Article  CAS  PubMed  Google Scholar 

  • Wang WW, Wang YF, Zhang SM, Xie KL, Zhang C, Xi YJ, Sun FL (2020) Genome-wide analysis of the abiotic stress-related bZIP family in switchgrass. Mol Biol Rep 47:4439–4454

    Article  CAS  PubMed  Google Scholar 

  • Wang XL, Chen X, Yang TB, Cheng Q, Cheng ZM (2017) Genome-wide identification of bZIP family genes involved in drought and heat stresses in strawberry (Fragaria vesca). Int J Genom 2017:3981031

    Google Scholar 

  • Wei KF, Chen J, Wang YM, Chen YH, Chen SX, Lin YN, Pan S, Zhong XJ, Xie DX (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ 38:35–49

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61:672–685

    Article  CAS  PubMed  Google Scholar 

  • Zhu SY, Yu XC, Wang XJ, Zhao R, Li Y, Fan RC, Shang Y, Du SY, Wang XF, Wu FQ, Xu YH, Zhang XY, Zhang DP (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19:3019–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zong W, Tang N, Yang J, Peng L, Ma SQ, Xu Y, Li GL, Xiong LZ (2016) Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes. Plant Physiol 171:2810–2825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, 26 Hexing Road, Harbin, 150040, People’s Republic of China

    YaNan Jing, Yue Yu, Hanzeng Wang, Ye Wu & Chenghao Li

Authors
  1. YaNan Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yue Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanzeng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ye Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chenghao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chenghao Li.

Additional information

Publisher's Note

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

Project funding: The work was supported by the Fundamental Research Funds for the Central Universities of China (2572018CL04), the Innovation Project of State Key Laboratory of Tree Genetics and Breeding (2020A02), and the Heilongjiang Touyan Innovation Team Program (Tree Genetics and Breeding Innovation Team).

The online version is available at http://www.springerlink.com.

Corresponding editor: Tao Xu.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 48 kb)

Supplementary file2 (DOCX 862 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jing, Y., Yu, Y., Wang, H. et al. Genome-wide identification and expression analysis of the bZIP gene family in silver birch (Betula pendula Roth.). J. For. Res. 33, 1615–1636 (2022). https://doi.org/10.1007/s11676-022-01453-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11676-022-01453-w

Keywords

Search

Navigation