Abstract
Basic leucine zipper (bZIP) proteins, which function as transcription factors and play important regulatory roles in all eukaryotic organisms, have been identified and classified in plants based on the sequenced genomes of model species such as Arabidopsis thaliana and rice (Oryza sativa). However, far less is currently known about the evolutionary relationships and expression patterns of bZIP genes in nonmodel plants. In this study, we performed a genome-wide analysis and identified a total of 47 bZIP transcription factors from grape (Vitis vinifera L., cv PN40024). Phylogenetic analysis of grape bZIP transcription factors along with their Arabidopsis and rice counterparts indicated that they can be classified into 13 different groups. Furthermore, evolutionary analysis of the grape bZIP transcription factors demonstrated that segmental duplications have contributed substantially to the expansion of this family in grape. In addition, synteny analysis between grape and Arabidopsis suggested that some of the bZIP members were present in their most recent common ancestor and that the major expansion occurred before the divergence of the two species. Gene expression analysis of the grape bZIP transcription factor-encoding genes revealed tissue-specific, biotic and abiotic stress and hormone-responsive expression profiles. Taken together, the genome-wide identification and characterization of grape bZIP transcription factors provide insights into their evolutionary history and a resource for further functional characterization in the context of crop improvement and stress tolerance.
Similar content being viewed by others
References
Amoutzias G, Veron A, Weiner J, Robinson-Rechavi M, Bornberg-Bauer E, Oliver S, Robertson D (2007) One billion years of bZIP transcription factor evolution: conservation and change in dimerization and DNA-binding site specificity. Mol Biol Evol 24(3):827–835
Büttner M, Singh KB (1997) Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc Natl Acad Sci U S A 94(11):5961–5966
Barbosa EGG, Leite JP, Marin SRR, Marinho JP, Carvalho JFC, Fuganti-Pagliarini R, Farias JRB, Neumaier N, Marcelino-Guimarães FC, de Oliveira MCN (2013) Overexpression of the ABA-dependent AREB1 transcription factor from Arabidopsis thaliana improves soybean tolerance to water deficit. Plant Mol Biol Rep 31(3):719–730
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488
Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci U S A 103(45):17042–17047
Boneh U, Biton I, Zheng C, Schwartz A, Ben-Ari G (2012) Characterization of potential ABA receptors in Vitis vinifera. Plant Cell Rep 31(2):311–321
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):10
Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153(3):1398–1412
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55(395):225–236
Chuang C-F, Running MP, Williams RW, Meyerowitz EM (1999) The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana. Genes Dev 13(3):334–344
Corrêa LGG, Riaño-Pachón DM, Schrago CG, Dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS One 3(8):e2944
Deppmann CD, Alvania RS, Taparowsky EJ (2006) Cross-species annotation of basic leucine zipper factor interactions: insight into the evolution of closed interaction networks. Mol Biol Evol 23(8):1480–1492
Du H, Wang Y-B, Xie Y, Liang Z, Jiang S-J, Zhang S-S, Huang Y-B, Tang Y-X (2013) Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants. DNA Res 20(5):437–448
Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66(1):94–116
Ferreira RB, Monteiro SS, Piçarra-Pereira MA, Teixeira AR (2004) Engineering grapevine for increased resistance to fungal pathogens without compromising wine stability. Trends Biotechnol 22(4):168–173
Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants. New Phytol 183(3):557–564
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17(12):3470–3488
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(6):901–915
Gao M, Wang Q, Wan R, Fei Z, Wang X (2012) Identification of genes differentially expressed in grapevine associated with resistance to Elsinoe ampelina through suppressive subtraction hybridization. Plant Physiol Biochem 58:253–268
García MNM, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235(4):761–778
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
Guo R, Xu X, Carole B, Li X, Gao M, Zheng Y, Wang X (2013) Genome-wide identification, evolutionary and expression analysis of the aspartic protease gene superfamily in grape. BMC Genomics 14:554
He S, Shan W, Kuang J-f, Xie H, Xiao Y-y, Lu W-j, Chen J-y (2013) Molecular characterization of a stress-response bZIP transcription factor in banana. Plant Cell Tiss Org Cul 113(2):173–187
Hurst HC (1994) Transcription factors 1: bZIP proteins. Protein Profile 2(2):101–168
Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467
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(3):106–111
Kang J-y, Choi H-i, Im M-y, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14(2):343–357
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(1):74–86
Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acid Res 40(D1):D302–D305
Li HE, Xu Y, Xiao Y, Zhu ZG, Xie XQ, Zhao HQ, Wang YJ (2010) Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta 232(6):1325–1337
Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141(4):1167–1184
Liao Y, Zou H-F, Wei W, Hao Y-J, Tian A-G, Huang J, Liu Y-F, Zhang J-S, Chen S-Y (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
Licausi F, Giorgi F, Zenoni S, Osti F, Pezzotti M, Perata P (2010) Genomic and transcriptomic analysis of the AP2/ERF superfamily in Vitis vinifera. BMC Genomics 11(1):719
Liu C, Wu Y, Wang X (2012) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235(6):1157–1169
Mallappa C, Yadav V, Negi P, Chattopadhyay S (2006) A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. J Biol Chem 281(31):22190–22199
Meier I, Gruissem W (1994) Novel conserved sequence motifs in plant G-box binding proteins and implications for interactive domains. Nucleic Acid Res 22(3):470–478
Meng X, Zhao W, Lin R, Wang M, Peng Y (2005) Identification of a novel rice bZIP-type transcription factor gene, OsbZIP1, involved in response to infection of Magnaporthe grisea. Plant Mol Biol Rep 23(3):301–302
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432
Niggeweg R, Thurow C, Kegler C, Gatz C (2000) Tobacco transcription factor TGA2.2 is the main component of as-1-binding factor ASF-1 and is involved in salicylic acid- and auxin-inducible expression of as-1-containing target promoters. J Biol Chem 275(26):19897–19905
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
Paterson AH, Wang X, Tang H, Lee TH (2012) Synteny and genomic rearrangements. Plant Gen Diver 1:195–207
Peng S, Zhu Z, Zhao K, Shi J, Yang Y, He M, Wang Y (2013) A novel heat shock transcription factor, VpHsf1, from Chinese wild Vitis pseudoreticulata is involved in biotic and abiotic stresses. Plant Mol Biol Rep 31(1):240–247
Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521
Pires N, Dolan L (2010) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27(4):862–874
Pontier D, Miao ZH, Lam E (2001) Trans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses. Plant J 27(6):529–538
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite. Trends Genet 16(6):276–277
Riechmann J, Heard J, Martin G, Reuber L, Keddie J, Adam L, Pineda O, Ratcliffe O, Samaha R, Creelman R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95(11):5857–5864
Siberil Y, Doireau P, Gantet P (2001) Plant bZIP G-box binding factors. Eur J Biochem 268(22):5655–5666
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(6):1148–1156
Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res 20(4):403–423
Sohn KH, Lee SC, Jung HW, Hong JK, Hwang BK (2006) Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol Biol 61(6):897–915
Tak H, Mhatre M (2013) Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera. Protoplasma 250(1):333–345
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
This P, Lacombe T, Thomas MR (2006) Historical origins and genetic diversity of wine grapes. Trends Genet 22(9):511–519
Upreti K, Murti G (2010) Response of grape rootstocks to salinity: changes in root growth, polyamines and abscisic acid. Biol Plant 54(4):730–734
Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011a) 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(3):212–231
Wang LJ, Li SH (2006) Thermotolerance and related antioxidant enzyme activities induced by heat acclimation and salicylic acid in grape (Vitis vinifera L.) leaves. Plant Grow Reg 48(2):137–144
Wang N, Xiang Y, Fang L, Wang Y, Xin H, Li S (2013) Patterns of gene duplication and their contribution to expansion of gene families in grapevine. Plant Mol Biol Rep 31:852–861
Wang Y, Liu Y, He P, Chen J (1995) Evaluation of foliar resistance to Uncinula necator in Chinese wild Vitis species. Vitis 34(3):159–164
Wang Y, Wang X, Tang H, Tan X, Ficklin SP, Feltus FA, Paterson AH (2011b) Modes of gene duplication contribute differently to genetic novelty and redundancy, but show parallels across divergent angiosperms. PLoS One 6(12):e28150
Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148(4):1938–1952
Xiao HG, Nassuth A (2006) Stress- and development-induced expression of spliced and unspliced transcripts from two highly similar dehydrin 1 genes in V. riparia and V. vinifera. Plant Cell Rep 25(9):968–977
Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2012) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276
Yang D-L, Yang Y, He Z (2013) Role of plant hormones and their cross-talks in rice immunity. Mol Plant 6:675–685
Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59(4):839–848
Zhang Y, Mao L, Wang H, Brocker C, Yin X, Vasiliou V, Fei Z, Wang X (2012) Genome-wide identification and analysis of grape aldehyde dehydrogenase (ALDH) gene superfamily. PloS One 7(2):e32153
Zhuang J, Peng R, Cheng Z, Zhang J, Cai B, Zhang Z, Gao F, Zhu B, Fu X, Jin X (2009) Genome-wide analysis of the putative AP2/ERF family genes in Vitis vinifera. Sci Hortic 123(1):73–81
Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66(6):675–683
Acknowledgments
The authors thank Dr. Yi Zheng for providing help with bioinformatics analysis. This work was supported by the National Natural Science Foundation of China grant no. 31272136 and the Program for Innovative Research Team of Grape Germplasm Resources and Breeding grant no. 2013KCT-25 to X.W.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gao, M., Zhang, H., Guo, C. et al. Evolutionary and Expression Analyses of Basic Zipper Transcription Factors in the Highly Homozygous Model Grape PN40024 (Vitis vinifera L.). Plant Mol Biol Rep 32, 1085–1102 (2014). https://doi.org/10.1007/s11105-014-0723-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-014-0723-3