Abstract
Homeodomain-Leu zipper (HD-Zip) gene family performs important biological functions related to organ development, photomorphogenesis and abiotic stress response in higher plants. However, systematic analysis of HD-Zip genes in Brassica rapa has not been performed. In the present study, a bioinformatics approach was used to identify and characterize the BraHD-Zip gene family in B. rapa. A total of 88 members were identified. All putative BraHD-Zip proteins contained a clear HD and LZ combined domain. Eighty-seven BraHD-Zips were non-randomly located on ten chromosomes. This gene family was mainly expanded following the whole genome triplication event and was preferentially over-retained relative to its neighboring genes in B. rapa. On phylogenetic analysis, the BraHD-Zips could be categorized into four distinct major groups (I–IV). Each group exhibited variant gene structures and motif distributions. Some syntenic orthologous gene pairs presented diverse expression profiles, which indicate that these gene pairs may be involved in the development of new functions during evolution. In summary, our analysis provided genome-wide insights into the expansion, preferential retention, expression profiles and functional diversity of BraHD-Zip genes following whole genome triplication in B. rapa.
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Agalou A, Purwantomo S, Overnas E, Johannesson H, Zhu X, Estiati A, de Kam RJ, Engstrom P, Slamet IH, Zhu Z, Wang M, Xiong L, Meijer AH, Ouwerkerk PB (2008) A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members. Plant Mol Biol 66(1–2):87–103
Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12(9):419–426
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–208
Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I, Giorgio M (2001) The Arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126:643–655
Carabelli M, Turchi L, Ruzza V, Morelli G, Ruberti I (2013) Homeodomain-Leucine Zipper II family of transcription factors to the limelight: central regulators of plant development. Plant Signal Behav 8 (9):e25447
Chen X, Chen Z, Zhao H, Zhao Y, Cheng B, Xiang Y (2014) Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PLoS One 9(2):e87156
Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136
Cheng F, Wu J, Fang L, Sun SL, Liu B, Lin K, Bonnema G, Wang XW (2012a) Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS One 7 (5):e36442
Cheng F, Wu J, Fang L, Wang X (2012b) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198
Ciarbelli AR, Ciolfi A, Salvucci S, Ruzza V, Possenti M, Carabelli M, Fruscalzo A, Sessa G, Morelli G, Ruberti I (2008) The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol Biol 68(4–5):465–478
Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9(12):938–950
Duan W, Song X, Liu T, Huang Z, Ren J, Hou X, Du J, Li Y (2015) Patterns of evolutionary conservation of ascorbic acid-related genes following whole-genome triplication in Brassica rapa. Genome Biol Evol 7(1):299–313
Freeling M, Thomas BC (2006) Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res 16(7):805–814
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186
Henriksson E, Olsson AS, Johannesson H, Johansson H, Hanson J, Engstrom P, Soderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis. Expression patterns and phylogenetic relationships. Plant Physiol 139(1):509–518
Hu R, Chi X, Chai G, Kong Y, He G, Wang X, Shi D, Zhang D, Zhou G (2012) Genome-wide identification, evolutionary expansion, and expression profile of homeodomain-leucine zipper gene family in poplar (Populus trichocarpa). PLoS One 7(2):e31149
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297
Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M (1999) ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 11(7):1217–1226
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40(D1):D1202–D1210
Lim SD, Yim WC, Moon JC, Kim DS, Lee BM, Jang CS (2010) A gene family encoding RING finger proteins in rice: their expansion, expression diversity, and co-expressed genes. Plant Mol Biol 72(4–5):369–380
Lou P, Wu J, Cheng F, Cressman LG, Wang X, McClung CR (2012) Preferential retention of circadian clock genes during diploidization following whole genome triplication in Brassica rapa. Plant Cell 24(6):2415–2426
Michael B, Eisen PTS, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 95(25):14863–14868
Nakamura M, Katsumata H, Abe M, Yabe N, Komeda Y, Yamamoto KT, Takahashi T (2006) Characterization of the class IV homeodomain-Leucine Zipper gene family in Arabidopsis. Plant Physiol 141(4):1363–1375
Olsson A, Engström P, Söderman E (2004) The homeobox genes ATHB12 and ATHB7 encode potential regulators of growth in response to water deficit in Arabidopsis. Plant Mol Biol 55(5):663–677
Park MY, Kim SA, Lee SJ, Kim SY (2013) ATHB17 is a positive regulator of abscisic acid response during early seedling growth. Mol Cells 35(2):125–133
Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23(9):1061–1067
Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17(1):61–76
Project BrGS (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035–1039
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37(5):501–506
Sessa G, Morelli G, Ruberti I (1997) DNA-binding specificity of the homeodomain-leucine zipper domain. J Mol Biol 274(3):303–309
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
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. Nucleic Acids Res 25(24):4876–4882
Tong CB, Wang XW, Yu JY, Wu J, Li WS, Huang JY, Dong CH, Hua W, Liu SY (2013) Comprehensive analysis of RNA-seq data reveals the complexity of the transcriptome in Brassica rapa. BMC Genomics 14(1):689
Torrent BJ, Martret SM, Brandt R, Musielak T, Palauqui JC, Martinez-Garcia JF, Wenkel S (2012) ATHB4 and HAT3, two class II HD-ZIP transcription factors, control leaf development in Arabidopsis. Plant Signal Behav 7(11):1382–1387
Victor M, Zúñiga M, Martinez NM, Folter SD (2012) The class II HD-ZIP JAIBA gene is involved in meristematic activity and important for gynoecium and fruit development in Arabidopsis. Plant Signal Behav 7(11):1–3
Wang Y, Henriksson E, So¨derman E, Henriksson KN, Sundberg E, Engstro¨m P (2003) The Arabidopsis homeobox gene, ATHB16, regulates leaf development and the sensitivity to photoperiod in Arabidopsis. Dev Biol 264:228–239
Zhang Z, Li J, Zhao X-Q, Wang J, Wong GK-S, Yu J (2006) KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinform 4(4):259–263
Zhang Z, Xiao J, Wu J, Zhang H, Liu G, Wang X, Dai L (2012) ParaAT: a parallel tool for constructing multiple protein-coding DNA alignments. Biochem Biophys Res Commun 419(4):779–781
Zhao Y, Zhou YQ, Jiang HY, Li XY, Gan DF, Peng XJ, Zhu SW, Cheng BJ (2011) Systematic analysis of sequences and expression patterns of drought-responsive members of the HD-Zip Gene family in maize. PLoS One 6(12):e28488
Acknowledgements
This work was supported by State Key Special Program “Seven Main Crops Breeding” (2016YFD0101701), National Science and Technology Support Program (2012BAD02B01), Independent Innovation of Agricultural Science and Technology Program of Jiangsu Province [CX(13)2006], Science and technology support program of Jiangsu Province (BE2013429), A Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions, National Natural Science Foundation of China (No. 31330067).
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10725_2017_268_MOESM1_ESM.eps
Fig. S1. Distribution of HD-Zip genes on chromosomes of Brassica rapa and Arabidopsis thaliana. (A) B. rapa chromosomes. (B) A. thaliana chromosomes. The synteny blocks are labeled on left of chromosomes (A to X). (EPS 1046 KB)
10725_2017_268_MOESM2_ESM.eps
Fig. S2. Prediction of physical/chemical characteristics of HD-Zip transcription factors family in eudicots. (A) Theoretical isoelectric point (pI). (B) Molecular weight (Mw). (EPS 548 KB)
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Fig. S4. An analytical view of the HD-Zip gene family in Brassica rapa. (A) Protein phylogenetic tree: The phylogenetic tree was constructed from a complete alignment of 88 BraHD-Zip proteins by maximum likelihood (ML) method with 1,000 bootstrap replicates using MEGA5.0. (B) Gene structure: Exon/intron structures of HD-Zip genes were drew by GSDS 2.0. Exons were represented by yellow boxes and introns by black lines. The sizes of exons and introns could be estimated using the scale below. (C) Protein structure: Schematic distributions of the conserved motifs among defined gene clusters. Motifs were identified by MEME software. The relative position of each identified motif in all HD-Zip proteins is shown. Multilevel consensus sequences for the MEME defined motifs were listed in Table S6. (EPS 3204 KB)
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Fig. S5. Heatmap of the expression profiles for HD-Zip genes across different tissues in Arabidopsis thaliana and Brassica rapa. (A) The A. thaliana expression profiling was analyzed using the AtGenExpress Visualization Tool with mean-normalized values (supplementary Table S10). (B) Gene expression FPKM values of RNA-Seq data were analyzed for Brassica rapa HD-Zip genes (supplementary Table S7). The color bar at the bottom of heat map represents relative expression values. (EPS 1065 KB)
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Jing, Z., Duan, W., Song, X. et al. Preferential retention, expression profile and potential functional diversity analysis of HD-Zip gene family in Brassica rapa . Plant Growth Regul 82, 421–430 (2017). https://doi.org/10.1007/s10725-017-0268-1
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DOI: https://doi.org/10.1007/s10725-017-0268-1