Plant Growth Regulation

, Volume 87, Issue 2, pp 227–243 | Cite as

Comparative identification, characterization, and expression analysis of bZIP gene family members in watermelon and melon genomes

  • Necdet Mehmet Unel
  • Fadime Cetin
  • Yasin Karaca
  • Yasemin Celik Altunoglu
  • Mehmet Cengiz BalogluEmail author
Original paper


The family of basic leucine zipper (bZIP) transcription factors plays diverse crucial roles in numerous biological processes. Despite the identification of bZIP genes in several plants, to our knowledge, bZIP members in watermelon and melon are yet to be comprehensively investigated. The genomes of watermelon and melon encode 59 ClabZIP and 75 CmbZIP putative genes, respectively. Both bZIP protein family members were phylogenetically grouped into seven subfamilies. The majority of bZIP genes in the same subfamily shared similar gene structures and conserved motifs. Chromosome distribution and genetic analysis revealed that 21 duplication events between ClabZIP genes and 106 duplication events between CmbZIP genes have occurred. Further, the three-dimensional structure and functional annotation of bZIP proteins was predicted. For evaluating the expression patterns of ClabZIP and CmbZIP genes, RNA-seq data available in public databases were analyzed. The expression profiles of selected ClabZIP and CmbZIP genes in root and leaf tissues of drought-stressed watermelon and melon were also examined using qRT-PCR. ClabZIP-57, CmbZIP-52, and CmbZIP-31 genes exhibited the highest expression levels after stress exposure in leaf and root tissues. Gene identification studies like the present study offer new perspectives in the analysis of bZIP protein family members and their functions in plants.


Cucumis melo Citrullus lanatus bZIP transcription factor genes Bioinformatics analysis Drought stress Gene expression analysis 


Author contributions

YCA and MCB conceived the study. FC, NMU and YK performed the experiments and carried out the analysis. YCA and MCB wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

10725_2018_465_MOESM1_ESM.pdf (3.4 mb)
Supplementary material 1 (PDF 3525 KB)


  1. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942CrossRefGoogle Scholar
  2. Bai Y et al (2016) Genome-wide analysis of the bZIP gene family identifies two ABI5-like bZIP transcription factors, BrABI5a and BrABI5b, as positive modulators of ABA signalling in Chinese cabbage. PLoS ONE. Google Scholar
  3. Bailey TL et al (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. CrossRefGoogle Scholar
  4. Baloglu MC (2014) Genome-wide in silico identification and comparison of Growth Regulating Factor (GRF) genes in Cucurbitaceae family. Plant Omics 7:260–270Google Scholar
  5. Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE. Google Scholar
  6. Berman HM et al (2000) The protein data bank. Nucleic Acids Res 28:235–242. CrossRefGoogle Scholar
  7. Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21:1280–1281. CrossRefGoogle Scholar
  8. Celik Altunoglu Y, Baloglu P, Yer EN, Pekol S, Baloglu MC (2016) Identification and expression analysis of LEA gene family members in cucumber genome. Plant Growth Regul 80:225–241. CrossRefGoogle Scholar
  9. Celik Altunoglu Y, Baloglu MC, Baloglu P, Yer EN, Kara S (2017) Genome-wide identification and comparative expression analysis of LEA genes in watermelon and melon genomes. Physiol Mol Biol Plants. Google Scholar
  10. Ciceri P, Locatelli F, Genga A, Viotti A, Schmidt RJ (1999) The activity of the maize Opaque2 transcriptional activator is regulated diurnally. Plant Physiol 121:1321–1327CrossRefGoogle Scholar
  11. Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics. Google Scholar
  12. Food and Agriculture Organization of the United Nations (FAO) (2014) FAOstat, statistical databases. Last updated 15 Aug 2014.
  13. Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915. CrossRefGoogle Scholar
  14. Garcia-Mas J et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci 109:11872–11877. CrossRefGoogle Scholar
  15. 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 60:207–217. CrossRefGoogle Scholar
  16. Guo S et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58CrossRefGoogle Scholar
  17. Hsieh T-H, Li C-W, Su R-C, Cheng C-P, Tsai Y-C, Chan M-T (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473. CrossRefGoogle Scholar
  18. Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. CrossRefGoogle Scholar
  19. Hu W et al (2016) Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep 6:22783. CrossRefGoogle Scholar
  20. Huang S et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281CrossRefGoogle Scholar
  21. Huang X-S, Liu J-H, Chen X-J (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 10:230–230. CrossRefGoogle Scholar
  22. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285. CrossRefGoogle Scholar
  23. 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. CrossRefGoogle Scholar
  24. Jin J, Zhang H, Kong L, Gao G, Luo J (2014a) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187. CrossRefGoogle Scholar
  25. Jin Z, Xu W, Liu A (2014b) Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta 239:299–312. CrossRefGoogle Scholar
  26. Kavas M, Kizildogan A, Gokdemir G, Baloglu MC (2015) Genome-wide investigation and expression analysis of AP2-ERF gene family in salt tolerant common bean. EXCLI J 14:1187–1206. Google Scholar
  27. Kavas M, Baloglu MC, Atabay ES, Ziplar UT, Dasgan HY, Unver T (2016) Genome-wide characterization and expression analysis of common bean bHLH transcription factors in response to excess salt concentration. Mol Genet Genomics 291:129–143. CrossRefGoogle Scholar
  28. Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371CrossRefGoogle Scholar
  29. Kobayashi F, Maeta E, Terashima A, Takumi S (2008) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134:74–86. CrossRefGoogle Scholar
  30. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefGoogle Scholar
  31. Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Díaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011. CrossRefGoogle Scholar
  32. Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK (2006) Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta 224:1209–1225. CrossRefGoogle Scholar
  33. Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–W478. CrossRefGoogle Scholar
  34. Li D, Fu F, Zhang H, Song F (2015a) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genomics 16:771. CrossRefGoogle Scholar
  35. Li X et al (2015b) Genome-wide identification and evolutionary analyses of bZIP transcription factors in wheat and its relatives and expression profiles of anther development related TabZIP genes. BMC Genomics 16:976. CrossRefGoogle Scholar
  36. Li Y-Y, Meng D, Li M, Cheng L (2016) Genome-wide identification and expression analysis of the bZIP gene family in apple (Malus domestica) Tree Genet Genomes. Google Scholar
  37. Liao Y et al (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240. CrossRefGoogle Scholar
  38. 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. CrossRefGoogle Scholar
  39. Liu J-X, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909. CrossRefGoogle Scholar
  40. Liu J et al (2014) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15:281. CrossRefGoogle Scholar
  41. Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229:605–615. CrossRefGoogle Scholar
  42. Lucas TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking annual. Rev Plant Biol 57:203–232. CrossRefGoogle Scholar
  43. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. CrossRefGoogle Scholar
  44. 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. CrossRefGoogle Scholar
  45. Pourabed E, Ghane Golmohamadi F, Soleymani Monfared P, Razavi SM, Shobbar Z-S (2015) Basic leucine zipper family in barley: genome-wide characterization of members expression analysis. Mol Biotechnol 57:12–26. CrossRefGoogle Scholar
  46. Rodriguez-Uribe L, O’Connell MA (2006) A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris). J Exp Bot 57:1391–1398. CrossRefGoogle Scholar
  47. Shen H, Cao K, Wang X (2007) A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer. Biochem Biophys Res Commun 362:425–430. CrossRefGoogle Scholar
  48. Silveira AB, Gauer L, Tomaz JP, Cardoso PR, Carmello-Guerreiro S, Vincentz M (2007) The Arabidopsis AtbZIP9 protein fused to the VP16 transcriptional activation domain alters leaf and vascular development. Plant Sci 172:1148–1156. CrossRefGoogle Scholar
  49. Söding J (2005) Protein homology detection by HMM–HMM comparison. Bioinformatics 21:951–960. CrossRefGoogle Scholar
  50. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612. CrossRefGoogle Scholar
  51. Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53:144–153. CrossRefGoogle Scholar
  52. Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488. CrossRefGoogle Scholar
  53. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. CrossRefGoogle Scholar
  54. Walsh J, Waters CA, Freeling M (1998) The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade–sheath boundary. Genes Dev 12:208–218CrossRefGoogle Scholar
  55. Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang S-Y (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on SorghumF. J Integr Plant Biol 53:212–231. CrossRefGoogle Scholar
  56. Wang Z et al (2015) Genome-wide analysis of the basic leucine zipper (bZIP) transcription factor gene family in six legume genomes. BMC Genomics 16:1053. CrossRefGoogle Scholar
  57. Wei K et al (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476. CrossRefGoogle Scholar
  58. Weltmeier F et al (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143. CrossRefGoogle Scholar
  59. Wingender E et al (2001) The TRANSFAC system on gene expression regulation. Nucleic Acids Res 29:281–283. CrossRefGoogle Scholar
  60. Yang Z, Gu S, Wang X, Li W, Tang Z, Xu C (2008) Molecular evolution of the CPP-like gene family in plants: insights from comparative genomics of Arabidopsis and rice. J Mol Evol 67:266–277. CrossRefGoogle Scholar
  61. Yang O, Popova OV, Süthoff U, Lüking I, Dietz K-J, Golldack D (2009) The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55. CrossRefGoogle Scholar
  62. Yang Y-G, Lv W-T, Li M-J, Wang B, Sun D-M, Deng X (2013) Maize membrane-bound transcription factor Zmbzip17 is a key regulator in the cross-talk of ER quality control and ABA signaling. Plant Cell Physiol 54:2020–2033. CrossRefGoogle Scholar
  63. Yer EN, Baloglu MC, Ziplar UT, Ayan S, Unver T (2015) Drought-responsive Hsp70 gene analysis in Populus at genome-wide level plant. Mol Biol Rep 34:483–500. CrossRefGoogle Scholar
  64. Yilmaz A, Nishiyama MY, Fuentes BG, Souza GM, Janies D, Gray J, Grotewold E (2009) GRASSIUS: a platform for comparative regulatory genomics across the grasses. Plant Physiol 149:171–180. CrossRefGoogle Scholar
  65. Yoshida T et al (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. CrossRefGoogle Scholar
  66. Yun K-Y et al (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol. Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Genetics and Bioengineering, Faculty of Engineering and ArchitectureKastamonu UniversityKastamonuTurkey

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