Whole-genome and dispersed duplication, including transposed duplication, jointly advance the evolution of TLP genes in seven representative Poaceae lineages

Chen, Huilong; Zhang, Yingchao; Feng, Shuyan

doi:10.1186/s12864-023-09389-z

Whole-genome and dispersed duplication, including transposed duplication, jointly advance the evolution of TLP genes in seven representative Poaceae lineages

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Published: 30 May 2023

Volume 24, article number 290, (2023)
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Whole-genome and dispersed duplication, including transposed duplication, jointly advance the evolution of TLP genes in seven representative Poaceae lineages

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Huilong Chen^1,2,
Yingchao Zhang¹ &
Shuyan Feng¹

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Abstract

Background

In the evolutionary study of gene families, exploring the duplication mechanisms of gene families helps researchers understand their evolutionary history. The tubby-like protein (TLP) family is essential for growth and development in plants and animals. Much research has been done on its function; however, limited information is available with regard to the evolution of the TLP gene family. Herein, we systematically investigated the evolution of TLP genes in seven representative Poaceae lineages.

Results

Our research showed that the evolution of TLP genes was influenced not only by whole-genome duplication (WGD) and dispersed duplication (DSD) but also by transposed duplication (TRD), which has been neglected in previous research. For TLP family size, we found an evolutionary pattern of progressive shrinking in the grass family. Furthermore, the evolution of the TLP gene family was at least affected by evolutionary driving forces such as duplication, purifying selection, and base mutations.

Conclusions

This study presents the first comprehensive evolutionary analysis of the TLP gene family in grasses. We demonstrated that the TLP gene family is also influenced by a transposed duplication mechanism. Several new insights into the evolution of the TLP gene family are presented. This work provides a good reference for studying gene evolution and the origin of duplication.

View this article's peer review reports

Evolutionary impact of whole genome duplication in Poaceae family

Article 28 July 2020

Phylogenomic profiles of whole-genome duplications in Poaceae and landscape of differential duplicate retention and losses among major Poaceae lineages

Article Open access 17 April 2024

Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants

Article Open access 21 February 2019

Introduction

Genes can be duplicated through a variety of mechanisms, including whole-genome duplication (WGD), tandem duplication (TD), proximal duplication (PD), dispersed duplication (DSD), and transposed duplication (TRD). Exploring the different duplication mechanisms of gene families helps us understand the origin and evolution of the genes and provides unique insights. By identifying the types of duplication origins of cold resistance genes in plants, Song et al. found that cold resistance genes can originate from singletons, DSD, PD, TD, and/or WGD and that WGD and DSD were the major contributors to gene duplication, thus proposing the hypothesis that cold resistance genes were preferentially retained after polyploidization events [1]. Liu et al. found that both WGD and TD played an important role in the expansion of intronless genes in intron-poor subfamilies by identifying the type of origin of duplication of intron-poor and intronless family genes in plants [2]. Nezamivand‑Chegin et al. proposed that WGD or DSD types were the most frequent contributors to SPX expansion by identifying the duplication types of SPX family genes in plants [3]. Therefore, it is useful to perform an analysis of the type of duplication origin of genes in evolutionary studies of gene families.

These duplication types are recognized by the duplicate_gene_classifier program in the MCScanX package and are divided into five types: singleton, WGD, TD, PD, and DSD [4, 5]. MCScanX enforces the determination that the origin of duplication of a gene can belong to only one of the five duplication types and does not allow a gene to originate through different duplication mechanisms. However, the true meaning of a singleton, as mentioned above, is that it does not undergo duplication; i.e., it should not be called a type of duplication. There are five types of gene duplication mechanisms: WGD, TD, PD, DSD, and TRD [5, 6]. Therefore, an important duplication mode (TRD) was missing in the above studies. TRD often leads to the formation of pseudogenes, while other types of duplication lead to rapid expansion of the plant genome [1, and the numbers 1–5 are cluster IDs, which are consistent with A, B

Full size image

According to the phylogenetic tree of the TLP genes, the genes of Clusters 1, 2, and 4 belong to the intron-rich clade, and the genes of Clusters 3 and 5 belong to the intron-poor clade (Figs. 3 and 5B, C). We found a high degree of consistency between the gene sets in each cluster and the phylogenetic tree. For example, Cluster 2 genes were all contained in Group F, and Cluster 1 genes were contained in adjacent Groups E, D, and C (Fig. 5B, C). The above phenomenon implies that the evolutionary pattern of grass TLP genes is one of conservation.

Homology clustering reflects species proximity and strong purifying selection

The identification of homologous genes in grasses showed that foxtail millet had the most orthologous gene pairs with the TLP gene family of green foxtail, and maize had the fewest orthologous gene pairs with the TLP gene families of barley and rice (Fig. 6A, Additional file 6: Table S5). This reflects the fact that the more closely related to each other the species are, the more TLP homologous gene pairs there are. The MCL homology clustering of grass TLP genes yielded 16 classes. Among them, there were four clusters containing genes from each species, and they showed single-copy gene patterns (Fig. 6A, Additional file 7: Table S6). Phylogenetic tree reconstruction and selection pressure on these four single-copy gene clusters showed that a total of 41 branches (95.35%, 43 branches in total) were subject to strong purifying selection (the ratio of the nonsynonymous to synonymous distances (ω) ranged from 0.0001 to 0.399558) (Fig. 6B), suggesting that grass TLP gene evolution has involved strong purifying selection.

Codon bias is weak and similar

To investigate whether codon usage bias has contributed to TLP gene evolution, we performed codon bias analysis on the TLP genes of each species using the CodonW program. The value of ENC denotes the number of effective codons and varies from 20 to 61; an ENC value less than 35 indicates strong codon bias [40, 41]. Our results show that the ENC values for the TLP gene family in each species are greater than 39 (Fig. 7A, Additional file 8: Tables S7, Additional file 9: S8), suggesting that the codon bias of the TLP genes is very weak.

ENC-GC3s plots were used to evaluate the influence of mutation selection on codon bias [40, 42]. Most of the TLP genes of the seven species were below and away from the standard curve (Fig. 7B), indicating a large difference between their actual and expected ENC values, suggesting that base mutations are not the main factor influencing their codon bias but that they may also be influenced by natural selection and other factors. A small number of genes were located at and near the standard curve, indicating that their actual ENC values were close to the expected values and suggesting that their codon bias is influenced by base mutations. Therefore, in conjunction with the previous selection pressure analysis, these findings indicate that base mutation and selection pressure jointly promoted the codon bias of TLP genes in the seven grass species, and purifying selection pressure may have a greater impact.

Regarding optimal codons, maize has 17 optimal codons, 1 of which ends in A and 16 of which end in G/C; sorghum has 13 optimal codons, 5 of which end in A/U and 8 of which end in G/C; foxtail millet has 18 optimal codons, 1 of which ends in A and 8 of which end in G/C; green foxtail has 14 optimal codons, 1 of which ends in A and 13 of which end in G/C; Brachypodium has 12 optimal codons, 0 of which end in A/U and 12 of which end in G/C; barley has 13 optimal codons, 1 of which ends in A and 12 of which end in G/C; and rice has 12 optimal codons, 0 of which end in A/U and 12 of which end in G/C (Fig. 8, Additional file 10: Table S9). These results imply that the optimal codon of the TLP gene family in all seven species prefers to end in C or G.

Venn network analysis showed that the seven grass TLP gene families share three optimal codons (AGG, AAG, and CAG). Maize shares a single optimal codon (GUC), sorghum shares four optimal codons (CAU, CCA, ACA, and GCU), grain shares three optimal codons (GCG, CAC, and ACG), barley shares one optimal codon (UGA) and rice shares one optimal codon (GGG) (Fig. 8, Additional file 11: Table S10). In summary, all results indicate that the codon biases of the seven species are nearly identical.

Discussion

Five mechanisms for the origin of gene duplication

MCScanX is often used to identify the type of origin of gene duplication in the evolutionary analysis of gene families [1,2,3, 35, 41, 43,44,45,46,47,48,49,50,51,87,88] was used to locate all possible k-clique communities for the TLP synteny network to identify communities (clusters of gene nodes) [38]. Then, the clustering results of the TLP synteny network (k = 3) were visualized in Cytoscape [89] to depict an undirected and unweighted network [39]. Finally, gene pairs in different clusters of the TLP synteny network were linked in a phylogenetic tree of the grass TLP gene family using iTOL [90] to perform phylogenetic profiling of clustered communities with differently coloured Bezier curves.

Inference of orthologues and selection pressure of single-copy gene clusters

The homology of the grass TLP family was inferred using OrthoMCL software (default parameters) [91]. Then, Cytoscape software was used to draw the lineal orthologous relationship network. Clustering analysis was performed using the Markov cluster (MCL) algorithm (− I > 1.5) [45, 92]. Single-copy clustered genes were used to construct the ML phylogenetic tree via FastTree [93], and the trees were then used to perform further maximum likelihood analysis using the Codeml program in PAML [94]. To detect whether a specific TLP gene had been positively selected, we compared two types of competing models, a free ratio model and a ratio-restriction model [95], following our previous steps [36, 56].

Codon bias and determination of optimal codons

To ensure the accuracy of the analysis, we analysed only the given CDSs with ATG (AUG) as the start codon, for which TAG (UAG), TGA (UGA), or TAA (UAA) was the stop codon, whose length was at least 300 bp and in which only A, T, C, and G bases were present [41]. The CodonW program (https://sourceforge.net/projects/codonw/) was used to analyse codon bias (default parameters), and the ENC-plot was created using the R package to detect the effect of base composition on codon bias, with the standard curve calculated as ENC = 2 + GC3s + 29/[GC3s2 + (1—GC3s)2] [40, 96]. Optimal codons for each species were determined as described in our previous studies [41]. Finally, optimal codons shared by different species were mined by Evenn [97].

Availability of data and materials

The datasets generated and/or analysed during the current study are available in this published article and the additional files.

Oryza sativa L. genome: the Rice Genome Annotation Project (RGAP) (http://rice.uga.edu/).

Zea mays Ensembl-18, Sorghum bicolor Rio v2.1, Setaria italica v2.2, Setaria viridis v2.1, Brachypodium distachyon Bd21-3 v1.1, and Hordeum vulgare r1 genome: the Phytozome database (https://phytozome-next.jgi.doe.gov/).

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Acknowledgements

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Funding

This research was supported by a PhD research start-up grant from North China University of Science and Technology (grant number 28424199).

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Authors and Affiliations

College of Life Sciences, North China University of Science and Technology, Tangshan, 063210, Hebei, China
Huilong Chen, Yingchao Zhang & Shuyan Feng
College of Grassland Science and Technology, China Agricultural University, Bei**g, 100193, China
Huilong Chen

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Huilong Chen
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Yingchao Zhang
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Shuyan Feng
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Contributions

The study was conceived by H.C.. H.C. and S.F. contributed to data collection and bioinformatics analysis. H.C. and Y.Z. participated in preparing and writing the manuscript. All authors contributed to revising the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Yingchao Zhang.

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Supplementary Information

Additional file 1: Table S1.

Patterns of TLP gene duplication origins and Ka/Ks in seven grass species.

Additional file 2: Table S2.

List of TLP genes in seven studied grass species.

Additional file 3: Figure S1.

Exon-intron distribution of all TLP genes in the seven grasses.

Additional file 4: Table S3.

Basic statistical details on structural elements of all TLP genes in seven grass species.

Additional file 5: Table S4.

Synteny network of TLPs in seven grass species.

Additional file 6: Table S5.

Orthologous network of TLPs in seven grass species.

Additional file 7: Table S6.

The cluster of TLP genes in seven grass species obtained using the MCL algorithm.

Additional file 8: Table S7.

Analysis of codon bias of TLP genes in seven grass species.

Additional file 9: Table S8.

Detailed parameter values for codon bias of eligible TLP genes in seven grass species.

Additional file 10: Table S9.

Optimal codons of TLP gene families in seven grass species.

Additional file 11: Table S10.

Venn calculation results of optimal codons for seven grass species.

Additional file 12: Figure S2.

The flowchart of DupGen_finder pipeline.

Additional file 13: Program S1.

Extraction of duplication gene pairs of family genes from all duplication gene pairs of a certain type in a species.

Additional file 14: Program S2.

Extraction of synteny networks of family genes from genome-wide synteny networks of all studied species.

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Chen, H., Zhang, Y. & Feng, S. Whole-genome and dispersed duplication, including transposed duplication, jointly advance the evolution of TLP genes in seven representative Poaceae lineages. BMC Genomics 24, 290 (2023). https://doi.org/10.1186/s12864-023-09389-z

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Received: 17 March 2023
Accepted: 18 May 2023
Published: 30 May 2023
DOI: https://doi.org/10.1186/s12864-023-09389-z

Whole-genome and dispersed duplication, including transposed duplication, jointly advance the evolution of TLP genes in seven representative Poaceae lineages

Abstract

Background

Results

Conclusions

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Introduction

Homology clustering reflects species proximity and strong purifying selection

Codon bias is weak and similar

Discussion

Five mechanisms for the origin of gene duplication

Inference of orthologues and selection pressure of single-copy gene clusters

Codon bias and determination of optimal codons

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