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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.


Model building of the 3D structure of Arabidopsis MATE protein AT1G73700. a, b Seven critical amino acid sites responsible for both functional divergence and positive selection and three sites responsible for coevolution are shown to a varying degree. The figure was produced using the Phyre2 and pyMOL programs. Sites responsible for both functional divergence and positive selection are colored red, while three responsible for coevolution are colored cyan
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Fig6: Model building of the 3D structure of Arabidopsis MATE protein AT1G73700. a, b Seven critical amino acid sites responsible for both functional divergence and positive selection and three sites responsible for coevolution are shown to a varying degree. The figure was produced using the Phyre2 and pyMOL programs. Sites responsible for both functional divergence and positive selection are colored red, while three responsible for coevolution are colored cyan

Mentions: We identified a group of amino acids showing coevolution in rice and another in Arabidopsis (Additional file 19). As shown in Fig. 6, there are three critical sites in the Arabidopsis MATE coevolving amino acids: 34 V, 409Y, and 454 W. These sites are far apart, suggesting functional dependency between them. Interestingly, in the five critical sites in rice with coevolving amino acids (Fig. 7), three sites (103Q, 322R, and 328G) were highly proximal and the other sites (286G and 425P) were also spatially proximal; thus, compensatory mutations might maintain the stability of the local structure, which might also be an indicator of functional coevolution.Fig. 6


The similar and different evolutionary trends of MATE family occurred between rice and Arabidopsis thaliana
Model building of the 3D structure of Arabidopsis MATE protein AT1G73700. a, b Seven critical amino acid sites responsible for both functional divergence and positive selection and three sites responsible for coevolution are shown to a varying degree. The figure was produced using the Phyre2 and pyMOL programs. Sites responsible for both functional divergence and positive selection are colored red, while three responsible for coevolution are colored cyan
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig6: Model building of the 3D structure of Arabidopsis MATE protein AT1G73700. a, b Seven critical amino acid sites responsible for both functional divergence and positive selection and three sites responsible for coevolution are shown to a varying degree. The figure was produced using the Phyre2 and pyMOL programs. Sites responsible for both functional divergence and positive selection are colored red, while three responsible for coevolution are colored cyan
Mentions: We identified a group of amino acids showing coevolution in rice and another in Arabidopsis (Additional file 19). As shown in Fig. 6, there are three critical sites in the Arabidopsis MATE coevolving amino acids: 34 V, 409Y, and 454 W. These sites are far apart, suggesting functional dependency between them. Interestingly, in the five critical sites in rice with coevolving amino acids (Fig. 7), three sites (103Q, 322R, and 328G) were highly proximal and the other sites (286G and 425P) were also spatially proximal; thus, compensatory mutations might maintain the stability of the local structure, which might also be an indicator of functional coevolution.Fig. 6

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.