Abstract
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.
Similar content being viewed by others
References
Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942
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. https://doi.org/10.1371/journal.pone.0158966
Bailey TL et al (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208. https://doi.org/10.1093/nar/gkp335
Baloglu MC (2014) Genome-wide in silico identification and comparison of Growth Regulating Factor (GRF) genes in Cucurbitaceae family. Plant Omics 7:260–270
Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE. https://doi.org/10.1371/journal.pone.0096014
Berman HM et al (2000) The protein data bank. Nucleic Acids Res 28:235–242. https://doi.org/10.1093/nar/28.1.235
Caraux G, Pinloche S (2005) PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 21:1280–1281. https://doi.org/10.1093/bioinformatics/bti141
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. https://doi.org/10.1007/s10725-016-0160-4
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. https://doi.org/10.1007/s12298-016-0405-8
Ciceri P, Locatelli F, Genga A, Viotti A, Schmidt RJ (1999) The activity of the maize Opaque2 transcriptional activator is regulated diurnally. Plant Physiol 121:1321–1327
Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics. https://doi.org/10.1155/2008/619832
Food and Agriculture Organization of the United Nations (FAO) (2014) FAOstat, statistical databases. Last updated 15 Aug 2014. http://www.fao.org
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. https://doi.org/10.2307/3871218
Garcia-Mas J et al (2012) The genome of melon (Cucumis melo L.). Proc Natl Acad Sci 109:11872–11877. https://doi.org/10.1073/pnas.1205415109
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. https://doi.org/10.1111/j.1365-313X.2009.03948.x
Guo S et al (2013) The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet 45:51–58
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. https://doi.org/10.1007/s00425-010-1147-4
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. https://doi.org/10.1093/bioinformatics/btu817
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. https://doi.org/10.1038/srep22783
Huang S et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41:1275–1281
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. https://doi.org/10.1186/1471-2229-10-230
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. https://doi.org/10.1073/pnas.0408941102
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. https://doi.org/10.1016/S1360-1385(01)02223-3
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. https://doi.org/10.1093/nar/gkt1016
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. https://doi.org/10.1007/s00425-013-1979-9
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. https://doi.org/10.17179/excli2015-600
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. https://doi.org/10.1007/s00438-015-1095-6
Kelley LA, Sternberg MJE (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363–371
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. https://doi.org/10.1111/j.1399-3054.2008.01107.x
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
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. https://doi.org/10.1074/jbc.M210538200
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. https://doi.org/10.1007/s00425-006-0302-4
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. https://doi.org/10.1093/nar/gkr201
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. https://doi.org/10.1186/s12864-015-1990-6
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. https://doi.org/10.1186/s12864-015-2196-7
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. https://doi.org/10.1007/s11295-016-1043-6
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. https://doi.org/10.1007/s00425-008-0731-3
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. https://doi.org/10.1186/s12864-015-1457-9
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. https://doi.org/10.1111/j.1365-313X.2007.03195.x
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. https://doi.org/10.1186/1471-2164-15-281
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. https://doi.org/10.1007/s00425-008-0857-3
Lucas TJ, Lucas WJ (2006) Integrative plant biology: role of phloem long-distance macromolecular trafficking annual. Rev Plant Biol 57:203–232. https://doi.org/10.1146/annurev.arplant.56.032604.144145
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155. https://doi.org/10.1126/science.290.5494.1151
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. https://doi.org/10.1104/pp.107.112821
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. https://doi.org/10.1007/s12033-014-9797-2
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. https://doi.org/10.1093/jxb/erj118
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. https://doi.org/10.1016/j.bbrc.2007.08.026
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. https://doi.org/10.1016/j.plantsci.2007.03.003
Söding J (2005) Protein homology detection by HMM–HMM comparison. Bioinformatics 21:951–960. https://doi.org/10.1093/bioinformatics/bti125
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. https://doi.org/10.1093/nar/gkl315
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. https://doi.org/10.1093/pcp/pcr157
Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488. https://doi.org/10.1126/science.1153917
Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. https://doi.org/10.1093/jhered/93.1.77
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 12:208–218
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. https://doi.org/10.1111/j.1744-7909.2010.01017.x
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. https://doi.org/10.1186/s12864-015-2258-x
Wei K et al (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476. https://doi.org/10.1093/dnares/dss026
Weltmeier F et al (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143. https://doi.org/10.1038/sj.emboj.7601206
Wingender E et al (2001) The TRANSFAC system on gene expression regulation. Nucleic Acids Res 29:281–283. https://doi.org/10.1093/nar/29.1.281
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. https://doi.org/10.1007/s00239-008-9143-z
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. https://doi.org/10.1016/j.gene.2009.02.010
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. https://doi.org/10.1093/pcp/pct142
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. https://doi.org/10.1007/s11105-015-0933-3
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. https://doi.org/10.1104/pp.108.128579
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. https://doi.org/10.1111/j.1365-313X.2009.04092.x
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. https://doi.org/10.1186/1471-2229-10-16
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Unel, N.M., Cetin, F., Karaca, Y. et al. Comparative identification, characterization, and expression analysis of bZIP gene family members in watermelon and melon genomes. Plant Growth Regul 87, 227–243 (2019). https://doi.org/10.1007/s10725-018-0465-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-018-0465-6