Abstract
The B-box proteins are a class of zinc finger transcription factors and play important roles in regulating plant growth, development, and stress response. However, their origin and expansion model in plants have been very vague. In this study, 208 B-box genes were identified in 18 plant species, and phylogenetic analyses divided them into five structure groups. Subsequently, the sequence analysis including theoretical isoelectric point, instability index, and aliphatic index showed the wide variation of B-box gene in different species. Our multispecies genome-wide analysis reveals that the structure groups III and IV in the plant BBX gene family have the earliest origin (Rhodophyta) and are extensively expanded in land plants, while the other three structure groups (I, II, and V) seem to originate at least in the last common ancestor of land plants. Furthermore, whole genome duplication (WGD) was the main driver (28 gene pairs, 65.12%) of the B-box gene family expansion, followed by segmental duplication, which tend to have more introns and are subject to more intense purification selections. We also analyzed the sequence differences between B-box domains to propose a new evolutionary model of B-box domain. These analyses provide new insights for understanding the origin and evolution of the B-box gene family.
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References
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Crocco CD, Botto JF (2013) BBX proteins in green plants: insights into their evolution, structure, feature and functional diversification. Gene 531:44–52. https://doi.org/10.1016/j.gene.2013.08.037
Crocco C, Holm M, Yanovsky MJ, Botto JF (2010) AtBBX21 and COP1 genetically interact in the regulation of shade avoidance. Plant J 64:551–562
Crocco CD, Holm M, Yanovsky MJ, Botto JF (2011) Function of B-BOX under shade. Plant Signal Behav 6:101–104. https://doi.org/10.4161/psb.6.1.14185
Ding L et al (2018) Two B-box domain proteins, BBX18 and BBX23, interact with ELF3 and regulate thermomorphogenesis in arabidopsis. Cell Rep 25:1718-1728 e1714. https://doi.org/10.1016/j.celrep.2018.10.060
Gangappa SN, Botto JF (2014) The BBX family of plant transcription factors. Trends Plant Sci 19:460–470
Huang J, Zhao X, Weng X, Wang L, Xie W, Phan LS (2012) The Rice B-box zinc finger gene family: genomic identification, characterization, expression profiling and diurnal analysis. PLoS ONE 7:e48242
Huang W, Xian Z, Kang X, Tang N, Li Z (2015) Genome-wide identification, phylogeny and expression analysis of GRAS gene family in tomato. BMC Plant Biol 15:209
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389:33–39
Khanna R, Kronmiller B, Maszle DR, Coupland G, Holm M, Mizuno T, Wu SH (2009) The Arabidopsis B-box zinc finger family. Plant Cell 21:3416–3420. https://doi.org/10.1105/tpc.109.069088
Lin F et al (2018) B-BOX DOMAIN PROTEIN28 negatively regulates photomorphogenesis by repressing the activity of transcription factor HY5 and undergoes COP1-mediated degradation. Plant Cell 30:2006–2019. https://doi.org/10.1105/tpc.18.00226
Liu X, Widmer A (2014) Genome-wide comparative analysis of the gras gene family in populus arabidopsis and rice. Plant Mol Biol Rep 32:1129–1145. https://doi.org/10.1007/s11105-014-0721-5
Liu B, Sun Y, Xue J, Jia X, Li R (2018) Genome-wide characterization and expression analysis of GRAS gene family in pepper (Capsicum annuum L.). PeerJ 6:e4796. https://doi.org/10.7717/peerj.4796
Massiah MA, Matts JA, Short KM, Simmons BN, Singireddy S, Yi Z, Cox TC (2007) Solution structure of the MID1 B-box2 CHC(D/C)C(2)H(2) zinc-binding domain: insights into an evolutionarily conserved RING fold. J Mol Biol 369:1–10. https://doi.org/10.1016/j.jmb.2007.03.017
Onouchi H, Igeño MI, Périlleux C, Coupland GG (2000) Mutagenesis of plants overexpressing CONSTANS demonstrates novel interactions among Arabidopsis flowering-time genes. Plant Cell Online 12:885–900
Qiu Y-L et al (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516
Quan SW et al (2019) Genome-wide identification classification, expression and duplication analysis of GRAS Family Genes in Juglans Regia L. Sci Rep 9:11643–11643
Samach A (2000) Distinct roles of CONSTANS target genes in reproductive development of arabidopsis. Science 288:1613–1616
Soitamo AJ, Piippo M, Allahverdiyeva Y, Battchikova N, Aro EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8:13. https://doi.org/10.1186/1471-2229-8-13
Song X et al (2020) The celery genome sequence reveals sequential paleo-polyploidizations, karyotype evolution and resistance gene reduction in apiales. Plant Biotechnol J. https://doi.org/10.1111/pbi.13499
Suárez-López P, Wheatley K, Robson F, Onouchi H, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120
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
Wang Y et al (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49. https://doi.org/10.1093/nar/gkr1293
Wang Q, Tu X, Zhang J, Chen X, Rao L (2013) Heat stress-induced BBX18 negatively regulates the thermotolerance in Arabidopsis. Mol Biol Rep 40:2679–2688. https://doi.org/10.1007/s11033-012-2354-9
Wang CY, Liu SS, Han GZ (2015) Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol 167(3):872
Wang J et al (2017) Hierarchically aligning 10 legume genomes establishes a family-level genomics platform. Plant Physiol 174:284–300. https://doi.org/10.1104/pp.16.01981
Wang J et al (2018a) An overlooked paleotetraploidization in cucurbitaceae. Mol Biol Evol 35:16–26. https://doi.org/10.1093/molbev/msx242
Wang JP et al (2018b) Two Likely auto-tetraploidization events shaped kiwifruit genome and contributed to establishment of the Actinidiaceae family. iScience 7:230–240. https://doi.org/10.1016/j.isci.2018.08.003
Xiong C et al (2019) A tomato B-box protein SlBBX20 modulates carotenoid biosynthesis by directly activating PHYTOENE SYNTHASE 1, and is targeted for 26S proteasome-mediated degradation. New Phytol 221:279–294. https://doi.org/10.1111/nph.15373
Yu L, Zhang G, Lyu Z, He C, Zhang J (2021) Genome-wide analysis of the GRAS gene family exhibited expansion model and functional differentiation in sea buckthorn (Hippophae rhamnoides L.). Plant Biotechnol Rep. https://doi.org/10.1007/s11816-021-00694-1
Acknowledgements
We would like to thank Mrs. H.M. Luo for their assistance with sample collection. We would also like to thank everyone who contributed to this manuscript in various capacities.
Funding
This research was funded by the National Natural Science Foundation of China [U2003116] and the Fundamental Research Funds for the Central Non-profit Research Institution of Chinese Academy of Forestry [No. ZDRIF2019; No. CAFYBB2020SZ001-2].
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CYH and JGZ supervised the research. LYY performed the experiments, analyzed the data, prepared figures and captions, and wrote the manuscript. GYZ and HL collected field samples. ZRL analyzed RNA-seq data. All of the authors have read and approve of the submitted manuscript.
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11816_2022_745_MOESM6_ESM.pdf
Figure S1 Gene structure of B-box genes. a The phylogenetic tree was constructed based on the full-length sequences of B-box proteins using MEGA 7 software. Details of clusters are shown in different colors. b Gene structure of B-box genes. Black line indicates intron, boxes of different colors are used to represent UTR, CDS, B-box domain, and CCT domain. Y-axis represents the subfamily name of each B-box genes. The lengths of the elements were drawn to scale
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Figure S2 Distribution of conserved motifs in B-box proteins. a The phylogenetic tree was constructed based on the full-length sequences of B-box proteins using MEGA 7 software. Details of clusters are shown in different colors. b The motif composition of B-box proteins. The motifs, numbers 1–10, are displayed in different-colored boxes. The length of protein can be estimated using the scale at the bottom
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Figure S3 Homologous collinear dot-plot within pineapple genome. The ID of the B-box gene is displayed at the edge. The collinearity blocks formed by the WGD are in green boxes in the figure, and the median value of Ks or the range of the median value of Ks of the collinearity blocks are marked
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Figure S4 Homologous collinear dot-plot within Ostreococcus lucimarinus genome. The ID of the B-box gene is displayed at the edge
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Figure S5 Homologous collinear dot-plot within Arabidopsis thaliana genome. The ID of the B-box gene is displayed at the edge. The collinearity blocks formed by the WGD are in green boxes in the figure, and the median value of Ks or the range of the median value of Ks of the collinearity blocks are marked
11816_2022_745_MOESM11_ESM.pdf
Figure S6 Homologous collinear dot-plot within Grape genome. The ID of the B-box gene is displayed at the edge. The collinearity blocks formed by the WGD are in green boxes in the figure, and the median value of Ks or the range of the median value of Ks of the collinearity blocks are marked
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Figure S7 Homologous collinear dot-plot within Rice genome. The ID of the B-box gene is displayed at the edge. The collinearity blocks formed by the WGD are in green boxes in the figure, and the median value of Ks or the range of the median value of Ks of the collinearity blocks are marked
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Figure S8 Homologous collinear dot-plot within Physcomitrella patens genome. The ID of the B-box gene is displayed at the edge. The collinearity blocks formed by the WGD are in green boxes in the figure, and the median value of Ks or the range of the median value of Ks of the collinearity blocks are marked
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Yu, L., Lyu, Z., Liu, H. et al. Insights into the evolutionary origin and expansion of the BBX gene family. Plant Biotechnol Rep 16, 205–214 (2022). https://doi.org/10.1007/s11816-022-00745-1
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DOI: https://doi.org/10.1007/s11816-022-00745-1