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The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana

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ABSTRACT

Background: Multidrug and toxic compound extrusion (MATE) transporter proteins are present in all organisms. Although the functions of some MATE gene family members have been studied in plants, few studies have investigated the gene expansion patterns, functional divergence, or the effects of positive selection.

Results: Forty-five MATE genes from rice and 56 from Arabidopsis were identified and grouped into four subfamilies. MATE family genes have similar exon-intron structures in rice and Arabidopsis; MATE gene structures are conserved in each subfamily but differ among subfamilies. In both species, the MATE gene family has expanded mainly through tandem and segmental duplications. A transcriptome atlas showed considerable differences in expression among the genes, in terms of transcript abundance and expression patterns under normal growth conditions, indicating wide functional divergence in this family. In both rice and Arabidopsis, the MATE genes showed consistent functional divergence trends, with highly significant Type-I divergence in each subfamily, while Type-II divergence mainly occurred in subfamily III. The Type-II coefficients between rice subfamilies I/III, II/III, and IV/III were all significantly greater than zero, while only the Type-II coefficient between Arabidopsis IV/III subfamilies was significantly greater than zero.

Results: A site-specific model analysis indicated that MATE genes have relatively conserved evolutionary trends. A branch-site model suggested that the extent of positive selection on each subfamily of rice and Arabidopsis was different: subfamily II of Arabidopsis showed higher positive selection than other subfamilies, whereas in rice, positive selection was highest in subfamily III. In addition, the analyses identified 18 rice sites and 7 Arabidopsis sites that were responsible for positive selection and for Type-I and Type-II functional divergence; there were no common sites between rice and Arabidopsis. Five coevolving amino acid sites were identified in rice and three in Arabidopsis; these sites might have important roles in maintaining local structural stability and protein functional domains.

Conclusions: We demonstrate that the MATE gene family expanded through tandem and segmental duplication in both rice and Arabidopsis. Overall, the results of our analyses contribute to improved understanding of the molecular evolution and functions of the MATE gene family in plants.

Electronic supplementary material: The online version of this article (doi:10.1186/s12870-016-0895-0) contains supplementary material, which is available to authorized users.

No MeSH data available.


Phylogenetic relationships and exon-intron structure of MATE genes. a A neighbor-joining (N-J) phylogenetic tree was constructed using the complete protein sequence alignments of 101 MATE genes identified using MUSCLE and MEGA6. Numbers at the nodes represent bootstrap support values (1000 replicates). The color of the subclades indicates the four gene subfamilies. b Exon-intron structures of the MATE genes. Boxes, exons; lines, introns. The lengths of boxes and lines are scaled according to gene length
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Fig3: Phylogenetic relationships and exon-intron structure of MATE genes. a A neighbor-joining (N-J) phylogenetic tree was constructed using the complete protein sequence alignments of 101 MATE genes identified using MUSCLE and MEGA6. Numbers at the nodes represent bootstrap support values (1000 replicates). The color of the subclades indicates the four gene subfamilies. b Exon-intron structures of the MATE genes. Boxes, exons; lines, introns. The lengths of boxes and lines are scaled according to gene length

Mentions: The program MUSCLE (Multiple Sequence Comparison by Log-Expectation) was employed to construct a multiple alignment of the identified 101 full-length protein sequences [27, 28]. The completed multiple alignment profiles of protein sequences were used to construct a phylogenetic tree with MEGA6.0 [29]. In addition, we employed three phylogenetic inference methods, namely neighbor-joining (N-J), minimum evolution (ME), and maximum likelihood (ML), to construct phylogenetic trees to confirm the topologies. All of these trees showed similar topologies; because the neighbor-joining (N-J) tree has higher bootstrap values than the other two phylogenetic trees. The N-J tree was employed for further analysis (Fig. 3). The topology of the N-J phylogenetic tree and the highest bootstrap values indicated that the MATE gene family could be divided into four major subfamilies: MATE I, MATE II, MATE III, and MATE IV. In order to explore the similarities and differences between members of the MATE gene family in rice and Arabidopsis, we constructed two N-J trees using the protein sequences of each species separately. Both trees had the same topology as that constructed using all 101 protein sequences (Additional files 7 and 8). All four MATE subgroups were present in both rice and Arabidopsis, indicating that these four subfamilies must have formed before the monocot-dicot split approximately 200 million years ago (Mya). The exon-intron organization of the MATE genes in the two species was examined by comparing the predicted coding sequences (CDSs) and their corresponding genomic sequences using GSDS software (http://gsds.cbi.pku.edu.cn/); this analysis was expected to provide more insight into the evolution of gene structures in the two species [30]. A majority of the genes of the MATE II subfamily (35 of 38; 92.1 %) had 6 to 8 introns (Fig. 3, Additional files 4 and 5). Similarly, 93.9 % (31 of 33) members of MATE I subfamily had 5 to 7 introns. However, all the genes in the MATE IV subfamily either lacked introns or had only a single intron; 13 genes had no introns and 6 genes had one intron. In contrast, 90.9 % (10 of 11) genes of MATE III subfamily had 11 to 13 introns: 5 genes had 11 introns, 2 genes had 12 introns, and 3 genes had 13 introns. Within the same subfamily, MATE genes of rice and Arabidopsis had similar intron numbers.Fig. 3


The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana
Phylogenetic relationships and exon-intron structure of MATE genes. a A neighbor-joining (N-J) phylogenetic tree was constructed using the complete protein sequence alignments of 101 MATE genes identified using MUSCLE and MEGA6. Numbers at the nodes represent bootstrap support values (1000 replicates). The color of the subclades indicates the four gene subfamilies. b Exon-intron structures of the MATE genes. Boxes, exons; lines, introns. The lengths of boxes and lines are scaled according to gene length
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5037600&req=5

Fig3: Phylogenetic relationships and exon-intron structure of MATE genes. a A neighbor-joining (N-J) phylogenetic tree was constructed using the complete protein sequence alignments of 101 MATE genes identified using MUSCLE and MEGA6. Numbers at the nodes represent bootstrap support values (1000 replicates). The color of the subclades indicates the four gene subfamilies. b Exon-intron structures of the MATE genes. Boxes, exons; lines, introns. The lengths of boxes and lines are scaled according to gene length
Mentions: The program MUSCLE (Multiple Sequence Comparison by Log-Expectation) was employed to construct a multiple alignment of the identified 101 full-length protein sequences [27, 28]. The completed multiple alignment profiles of protein sequences were used to construct a phylogenetic tree with MEGA6.0 [29]. In addition, we employed three phylogenetic inference methods, namely neighbor-joining (N-J), minimum evolution (ME), and maximum likelihood (ML), to construct phylogenetic trees to confirm the topologies. All of these trees showed similar topologies; because the neighbor-joining (N-J) tree has higher bootstrap values than the other two phylogenetic trees. The N-J tree was employed for further analysis (Fig. 3). The topology of the N-J phylogenetic tree and the highest bootstrap values indicated that the MATE gene family could be divided into four major subfamilies: MATE I, MATE II, MATE III, and MATE IV. In order to explore the similarities and differences between members of the MATE gene family in rice and Arabidopsis, we constructed two N-J trees using the protein sequences of each species separately. Both trees had the same topology as that constructed using all 101 protein sequences (Additional files 7 and 8). All four MATE subgroups were present in both rice and Arabidopsis, indicating that these four subfamilies must have formed before the monocot-dicot split approximately 200 million years ago (Mya). The exon-intron organization of the MATE genes in the two species was examined by comparing the predicted coding sequences (CDSs) and their corresponding genomic sequences using GSDS software (http://gsds.cbi.pku.edu.cn/); this analysis was expected to provide more insight into the evolution of gene structures in the two species [30]. A majority of the genes of the MATE II subfamily (35 of 38; 92.1 %) had 6 to 8 introns (Fig. 3, Additional files 4 and 5). Similarly, 93.9 % (31 of 33) members of MATE I subfamily had 5 to 7 introns. However, all the genes in the MATE IV subfamily either lacked introns or had only a single intron; 13 genes had no introns and 6 genes had one intron. In contrast, 90.9 % (10 of 11) genes of MATE III subfamily had 11 to 13 introns: 5 genes had 11 introns, 2 genes had 12 introns, and 3 genes had 13 introns. Within the same subfamily, MATE genes of rice and Arabidopsis had similar intron numbers.Fig. 3

View Article: PubMed Central - PubMed

ABSTRACT

Background: Multidrug and toxic compound extrusion (MATE) transporter proteins are present in all organisms. Although the functions of some MATE gene family members have been studied in plants, few studies have investigated the gene expansion patterns, functional divergence, or the effects of positive selection.

Results: Forty-five MATE genes from rice and 56 from Arabidopsis were identified and grouped into four subfamilies. MATE family genes have similar exon-intron structures in rice and Arabidopsis; MATE gene structures are conserved in each subfamily but differ among subfamilies. In both species, the MATE gene family has expanded mainly through tandem and segmental duplications. A transcriptome atlas showed considerable differences in expression among the genes, in terms of transcript abundance and expression patterns under normal growth conditions, indicating wide functional divergence in this family. In both rice and Arabidopsis, the MATE genes showed consistent functional divergence trends, with highly significant Type-I divergence in each subfamily, while Type-II divergence mainly occurred in subfamily III. The Type-II coefficients between rice subfamilies I/III, II/III, and IV/III were all significantly greater than zero, while only the Type-II coefficient between Arabidopsis IV/III subfamilies was significantly greater than zero.

Results: A site-specific model analysis indicated that MATE genes have relatively conserved evolutionary trends. A branch-site model suggested that the extent of positive selection on each subfamily of rice and Arabidopsis was different: subfamily II of Arabidopsis showed higher positive selection than other subfamilies, whereas in rice, positive selection was highest in subfamily III. In addition, the analyses identified 18 rice sites and 7 Arabidopsis sites that were responsible for positive selection and for Type-I and Type-II functional divergence; there were no common sites between rice and Arabidopsis. Five coevolving amino acid sites were identified in rice and three in Arabidopsis; these sites might have important roles in maintaining local structural stability and protein functional domains.

Conclusions: We demonstrate that the MATE gene family expanded through tandem and segmental duplication in both rice and Arabidopsis. Overall, the results of our analyses contribute to improved understanding of the molecular evolution and functions of the MATE gene family in plants.

Electronic supplementary material: The online version of this article (doi:10.1186/s12870-016-0895-0) contains supplementary material, which is available to authorized users.

No MeSH data available.