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Insights into the evolutionary origin and expansion of the BBX gene family

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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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All data analyzed during this study are included in this article and its Online Resource files.

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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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Correspondence to Caiyun He or Jianguo Zhang.

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Table S1 Genomic data information used in this study

Table S2 Information about the predicted structure of some BBX proteins

Table S3 Accession numbers and characteristics of 208 B-box genes

Table S4 Table S4 Calculation of Ka and Ks ratios of B-box gene pairs with different duplication model

Table S5 Classification of BBX genes in a new hypothetical model of B-box domain evolution

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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

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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

Figure S9 Alignment map of the full-length sequence of B-box domains in all B-box genes

Figure S10 Alignment map of the full-length sequence of CCT domains in all B-box genes

Figure S11 Alignment map of the B-box topology sequence in clade I (B2) of phylogenetic tree

Figure S12 Alignment map of the B-box topology sequence in clade II (B1) of phylogenetic tree

Figure S13 Alignment map of the B-box topology sequence in clade III (B2’) of phylogenetic tree

Figure S14 Phylogenetic tree was constructed based on the topology sequence of CCT domains

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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

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