Skip to main content
Log in

Genome-wide identification and expression analysis of the bZIP gene family in apple (Malus domestica)

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

The basic leucine zipper (bZIP) family is one of the largest transcription factor (TF) families in plants, which play crucial roles in plant growth and development. bZIP proteins are involved in multiple biological processes, as well as responses to various biotic/abiotic stresses. Although genome-wide analysis of the bZIP gene family has been conducted in several plant species, only few comprehensive characterization of this gene family has been reported in apple (Malus domestica), an important tree fruit in the Rosaceae family. In this study, we identified 114 bZIP genes from the apple genome, which were divided into 10 subgroups based on their sequences. We further characterized these MdbZIP genes in terms of gene structure, protein model, and chromosomal distribution. Genome-wide expression profile of MdbZIP genes indicated that 14 MdbZIPs were highly expressed during apple fruit development, and 17 MdbZIPs showed differential expression in leaves and mature apple fruit. Analysis of the expression of 16 MdbZIPs under drought and salt stresses in apple leaves and roots using quantitative real-time PCR (qRT-PCR) indicated that they all exhibited differential transcript levels in both treatments, suggesting that MdbZIP genes are involved in abiotic stress responses. The genome-wide identification, characterization, and expression analysis of apple bZIP genes provide new insights into the roles of the bZIP TF family and lay a solid foundation for future cloning and functional analysis of this gene family, which may be used to manipulate apple growth and development and improve its stress tolerance.

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
Fig. 9

Similar content being viewed by others

References

  • Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannonia JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17: 2954–2965. doi: 10.1105/tpc.105.036053

  • Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS One 9(4): e96014. doi:10.1371/journal.pone.0096014

  • Chen H, Chen W, Zhou J, He H, Chen L, Deng XW (2012) Basic leucine zipper transcription factor OsbZIP16 positively regulates drought resistance in rice. Plant Sci 193-194: 8–17. doi:10.1016/j.plantsci.2012.05.003

  • Chung MY, Vrebalov J, Alba R, Lee JM, McQuinn R, Chung JD, Klein P, Giovannoni JJ (2010) A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J 64:936–947. doi:10.1111/j.1365-313X.2010.04384.x

    Article  CAS  PubMed  Google Scholar 

  • Du H, Yang S, Liang Z, Feng B, Liu L, Huang Y, Tang Y (2012) Genome-wide analysis of the MYB transcription factor superfamily in soybean. BMC Plant Biol 12:106. doi:10.1186/1471-2229-12-106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellenberger TE, Brandl CJ, Struhl K, Harrison SC (1992) The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted a helices: crystal structure of the protein-DNA complex. Cell 71(7):1223–1237. doi:10.1016/S0092-8674(05)80070-4

    Article  CAS  PubMed  Google Scholar 

  • Gasic K, Hernandez A, Korban SS (2004) RNA Extraction from Different Apple Tissues Rich in Polyphenols and Polysaccharides for cDNA Library Construction. Plant Mol Biol Reporter 22:437--437. doi:10.1007/BF02772687

  • Guan Y, Ren H, Xie H, Ma Z, Chen F (2009) Identification and characterization of bZIP-type transcription factors involved in carrot (Daucus carota L.) somatic embryogenesis. Plant J 60(2):207–217. doi:10.1111/j.1365-313X.2009.03948.x

    Article  CAS  PubMed  Google Scholar 

  • Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230. doi:10.1186/1471-2229-10-230

    Article  PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Lee Y, Cho J, Ahn C, Lee S, Jeon J, Kang H, Lee C, An G, Park PB (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72:557–566. doi:10.1007/s11103-009-9592-9

    Article  Google Scholar 

  • Hsieh T, Li C, Su R, Cheng C, Sanjaya Tsai Y, Chan M (2012) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231(6):1459–1473. doi:10.1007/s00425-010-1147-4

    Article  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(9):1277–1287. doi:10.1105/tpc.6.9.1277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshhaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends in Plant Sci 7(3):106–111. doi:10.1016/S1360-1385(01)02223-3

    Article  CAS  Google Scholar 

  • Jin Z, Xu W, Liu A (2014) Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta 239:299–312. doi:10.1007/s00425-013-1979-9

    Article  CAS  PubMed  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(4860): 1759–1764. doi:10.1126/science.3289117

  • Li D, Fu F, Zhang H, Song F (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomic 16:771. doi:10.1186/s12864-015-1990-6

    Article  Google Scholar 

  • Liao Y, Zou HF, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228(2):225–240. doi:10.1007/s00425-008-0731-3

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Mao B, Ou S, Wang W, Liu L, Wu Y, Chu C, Wang X (2014b) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84(1–2):19–36. doi:10.1007/s11103-013-0115-3

    Article  CAS  PubMed  Google Scholar 

  • Liu GT, Wang JF, Cramer G, Dai ZW, Duan W, HG X, BH W, Fan PG, Wang LJ, Li SH (2012) Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biol 12:174. doi:10.1186/1471-2229-12-174

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Chu Z (2015) Genome-wide evolutionary characterization and analysis of bZIP transcription factors and their expression profiles in response to multiple abiotic stresses in Brachypodium distachyon. BMC Genomics 16:227. doi:10.1186/s12864-015-1457-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Chen N, Chen F, Cai B, Santo SD, Tornielli GB, Pezzotti M, Cheng Z (2014a) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15:281. doi:10.1186/1471-2164-15-281

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32(3):317–328. doi:10.1046/j.1365-313X.2002.01430.x

    Article  CAS  PubMed  Google Scholar 

  • Lovisetto A, Guzzo F, Tadiello A, Confortin E, Pavanello A, Botton A, Casadoro G (2013) Characterization of a bZIP gene highly expressed during ripening of the peach fruit. Plant Physiol Biochem 70:462–470. doi:10.1016/j.plaphy.2013.06.014

    Article  CAS  PubMed  Google Scholar 

  • Neill SJ, Burnett EC (1999) Regulation of gene expression during water deficit stress. Plant Growth Regul 29:23–33. doi:10.1023/A:1006251631570

    Article  CAS  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(2):333–350. doi:10.1104/pp.107.112821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:822–827. doi:10.1093/nar/gkp805

    Article  Google Scholar 

  • Rook F, Gerrits N, Kortstee A, van Kampen M, Borrias M, Weisbeek P, Smeekens S (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J 15:253–263. doi:10.1046/j.1365-313X.1998.00205.x

    Article  CAS  PubMed  Google Scholar 

  • Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T (2005) LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants. Plant Cell Physiol 46(10):1623–1634. doi:10.1093/pcp/pci178

    Article  CAS  PubMed  Google Scholar 

  • Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951–960. doi:10.1093/bioinformatics/bti125

    Article  PubMed  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerte-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, Mering C (2014) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucl Acids Res 1–6. doi:10.1093/nar/gku1003

  • Talanian RV, Mcknight CJ, Kim PS (1990) Sequence-specific DNA-binding by a short peptide dimer. Science 249:769–771. doi:10.1126/science.2389142

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725--2729. doi:10.1093/molbev/mst19

  • Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005) Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J 44(1):100–113. doi:10.1111/j.1365-313X.2005.02513.x

    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(5):556–558. doi:10.4161/psb.19839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udrardi MK, Czechowski T, Scheible WR (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20:1736–1737. doi:10.1105/tpc.108.061143

    Article  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana1 P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse V, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42(10): 833–841. doi:10.1038/ng.654

  • Walsh J, Freeling M (1999) The liguleless2 gene of maize functions during the transition from the vegetative to the reproductive shoot apex. Plant J 19(4):489–495. doi:10.1046/j.1365-313X.1999.00541.x

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang S (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J of Integrative Plant Biol 53(3):212–231. doi:10.1111/j.1744-7909.2010.01017.x

    Article  CAS  Google Scholar 

  • Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64(11):3453–3466. doi:10.1093/jxb/ert187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XL, Zhong Y, Cheng ZM, Xiong JS (2015) Divergence of the bZIP gene family in strawberry, peach, and apple suggests multiple modes of gene evolution after duplication. International Journal of Genomics 536943:11. doi:10.1155/2015/536943

    Google Scholar 

  • Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476. doi:10.1093/dnares/dss026

    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(5737):1056–1059. doi:10.1126/science.1114358

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Zhu Q, Dai S, Lamb C, Beachy RN (1997) RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development. EMBO J 16(17):5247–5259. doi:10.1093/emboj/16.17.5247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lailiang Cheng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

The apple bZIP gene family sequences have been submitted to GDR (Genome Database for Rosaceae), and the accession number been shown in the Table 1.

Additional information

Communicated by V. Decroocq

Yuan-Yuan Li and Dong Meng contributed equally to this work.

Electronic supplementary material

Fig. S1

Phylogenetic tree that added four reference’s bZIP apple genes (JPEG 153 kb)

High-resolution image (TIFF 1551 kb)

Fig. S2

Phylogenetic tree made by full length of bZIP proteins (JPEG 147 kb)

High-resolution image (TIFF 1461 kb)

Table S1

Quantitative real-time PCR primers for expression analysis of MdbZIP genes (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, YY., Meng, D., Li, M. et al. Genome-wide identification and expression analysis of the bZIP gene family in apple (Malus domestica). Tree Genetics & Genomes 12, 82 (2016). https://doi.org/10.1007/s11295-016-1043-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-016-1043-6

Keywords

Navigation