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

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.


Multiple sequence alignment of several MATE protein sequences. Sequence alignment of the reference proteins (LOC_Os01g49120 and AT1G73700) with NorM-NG, NorM-VC, NorM-VP, and hMATE1. Regions of transmembrane helices (TM) in LOC_Os01g49120 are outlined and numbered. Blue dots and triangles indicate amino acids responsible for functional divergence, positive selection and coevolution in the reference sequence AT1G73700. Red dots and triangles indicate amino acids responsible for functional divergence, positive selection, and coevolution in the reference sequence LOC_Os01g49120. The cyan and red outlined boxes represent amino acids that might coordinate cations and interact with substrates, respectively
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Fig8: Multiple sequence alignment of several MATE protein sequences. Sequence alignment of the reference proteins (LOC_Os01g49120 and AT1G73700) with NorM-NG, NorM-VC, NorM-VP, and hMATE1. Regions of transmembrane helices (TM) in LOC_Os01g49120 are outlined and numbered. Blue dots and triangles indicate amino acids responsible for functional divergence, positive selection and coevolution in the reference sequence AT1G73700. Red dots and triangles indicate amino acids responsible for functional divergence, positive selection, and coevolution in the reference sequence LOC_Os01g49120. The cyan and red outlined boxes represent amino acids that might coordinate cations and interact with substrates, respectively

Mentions: We identified 18 and 7 critical sites in rice and Arabidopsis, respectively, that were responsible for positive selection, and Type-I, and Type-II functional divergence (Figs. 6 and 7). These sites were located on the corresponding three-dimensional OsMATE and AtMATE structures. We performed a multiple sequence alignment to further investigate rice and Arabidopsis MATE protein functions (Fig. 8). Among the 18 identified rice critical sites, TM3 (transmembrane helices 3), L3-4 (linker between TM3 and TM4), and TM4 were observed at three sites each; L6-L7, L8-L9, and TM10 each had two critical sites; and TM8, TM11, and TM12 each had one critical site (Figs. 7 and 8). Among the 7 Arabidopsis critical sites, TM1 had two sites, and TM2, L6-7, TM7, TM11 each had one site; the C-terminus also had one site. The results suggested that these critical amino acids might make an important contribution to the adaptiveness of MATE proteins for different functional needs in rice and Arabidopsis.Fig. 8


The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana
Multiple sequence alignment of several MATE protein sequences. Sequence alignment of the reference proteins (LOC_Os01g49120 and AT1G73700) with NorM-NG, NorM-VC, NorM-VP, and hMATE1. Regions of transmembrane helices (TM) in LOC_Os01g49120 are outlined and numbered. Blue dots and triangles indicate amino acids responsible for functional divergence, positive selection and coevolution in the reference sequence AT1G73700. Red dots and triangles indicate amino acids responsible for functional divergence, positive selection, and coevolution in the reference sequence LOC_Os01g49120. The cyan and red outlined boxes represent amino acids that might coordinate cations and interact with substrates, respectively
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5037600&req=5

Fig8: Multiple sequence alignment of several MATE protein sequences. Sequence alignment of the reference proteins (LOC_Os01g49120 and AT1G73700) with NorM-NG, NorM-VC, NorM-VP, and hMATE1. Regions of transmembrane helices (TM) in LOC_Os01g49120 are outlined and numbered. Blue dots and triangles indicate amino acids responsible for functional divergence, positive selection and coevolution in the reference sequence AT1G73700. Red dots and triangles indicate amino acids responsible for functional divergence, positive selection, and coevolution in the reference sequence LOC_Os01g49120. The cyan and red outlined boxes represent amino acids that might coordinate cations and interact with substrates, respectively
Mentions: We identified 18 and 7 critical sites in rice and Arabidopsis, respectively, that were responsible for positive selection, and Type-I, and Type-II functional divergence (Figs. 6 and 7). These sites were located on the corresponding three-dimensional OsMATE and AtMATE structures. We performed a multiple sequence alignment to further investigate rice and Arabidopsis MATE protein functions (Fig. 8). Among the 18 identified rice critical sites, TM3 (transmembrane helices 3), L3-4 (linker between TM3 and TM4), and TM4 were observed at three sites each; L6-L7, L8-L9, and TM10 each had two critical sites; and TM8, TM11, and TM12 each had one critical site (Figs. 7 and 8). Among the 7 Arabidopsis critical sites, TM1 had two sites, and TM2, L6-7, TM7, TM11 each had one site; the C-terminus also had one site. The results suggested that these critical amino acids might make an important contribution to the adaptiveness of MATE proteins for different functional needs in rice and Arabidopsis.Fig. 8

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.