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Unusual tandem expansion and positive selection in subgroups of the plant GRAS transcription factor superfamily.

Wu N, Zhu Y, Song W, Li Y, Yan Y, Hu Y - BMC Plant Biol. (2014)

Bottom Line: All of tandem duplicated genes were found in group II except one cluster of rice, indicating that tandem duplication greatly promoted the expansion of group II.These results strongly indicated that these groups were experiencing higher positive selection pressure.In short, the results above provide a solid foundation for further functional dissection of the GRAS gene superfamily.

View Article: PubMed Central - PubMed

ABSTRACT

Background: GRAS proteins belong to a plant transcription factor family that is involved with multifarious roles in plants. Although previous studies of this protein family have been reported for Arabidopsis, rice, Chinese cabbage and other species, investigation of expansion patterns and evolutionary rate on the basis of comparative genomics in different species remains inadequate.

Results: A total of 289 GRAS genes were identified in Arabidopsis, B. distachyon, rice, soybean, S. moellendorffii, and P. patens and were grouped into seven subfamilies, supported by the similarity of their exon-intron patterns and structural motifs. All of tandem duplicated genes were found in group II except one cluster of rice, indicating that tandem duplication greatly promoted the expansion of group II. Furthermore, segment duplications were mainly found in the soybean genome, whereas no single expansion pattern dominated in other plant species indicating that GRAS genes from these five species might be subject to a more complex evolutionary mechanism. Interestingly, branch-site model analyses of positive selection showed that a number of sites were positively selected under foreground branches I and V. These results strongly indicated that these groups were experiencing higher positive selection pressure. Meanwhile, the site-specific model revealed that the GRAS genes were under strong positive selection in P. patens. DIVERGE v2.0 was used to detect critical amino acid sites, and the results showed that the shifted evolutionary rate was mainly attributed to the functional divergence between the GRAS genes in the two groups. In addition, the results also demonstrated the expression divergence of the GRAS duplicated genes in the evolution. In short, the results above provide a solid foundation for further functional dissection of the GRAS gene superfamily.

Conclusions: In this work, differential expression, evolutionary rate, and expansion patterns of the GRAS gene family in the six species were predicted. Especially, tandem duplication events played an important role in expansion of group II. Together, these results contribute to further functional analysis and the molecular evolution of the GRAS gene superfamily.

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Related in: MedlinePlus

Phylogenetic tree of GRAS proteins amongArabidopsis,Brachypodium distachyon, rice, soybean,Physcomitrella patens, andSelaginella moellendorffii. A) The major clusters of orthologous genes are shown in different colors: group I = purple, group II = dark blue, group III = yellow, group IV = light green, group V = pink, group VI = dark green, and group VII = light blue. The scale bar corresponds to 0.1 estimated amino acid substitutions per site; B) Genes belonging to the different groups are shown. Among them, the deduced DELLA proteins are indicated by a filled red square, and genes with similar functions clustered together are indicated by filled green circles.
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Fig1: Phylogenetic tree of GRAS proteins amongArabidopsis,Brachypodium distachyon, rice, soybean,Physcomitrella patens, andSelaginella moellendorffii. A) The major clusters of orthologous genes are shown in different colors: group I = purple, group II = dark blue, group III = yellow, group IV = light green, group V = pink, group VI = dark green, and group VII = light blue. The scale bar corresponds to 0.1 estimated amino acid substitutions per site; B) Genes belonging to the different groups are shown. Among them, the deduced DELLA proteins are indicated by a filled red square, and genes with similar functions clustered together are indicated by filled green circles.

Mentions: Comparison of conserved motifs among members of the GRAS family implied that they can be divided into different groups and subgroups. To better separate the groups and investigate the evolutionary relationships among GRAS proteins in Arabidopsis, B. distachyon, rice, soybean, S. moellendorffii, and P. patens, an unrooted phylogenetic tree was constructed from 289 full-length amino acid sequences using the neighbor-joining (NJ) algorithm (Figure 1 and Additional file 10). To confirm the tree topologies, a ML (maximum likelihood) phylogenetic tree was also constructed, and it showed similar topology to the NJ tree with only minor modifications (Additional file 11). A ME (Minimum-Evolution) phylogenetic tree was also constructed, which showed the same topology to the NJ tree (Additional file 12). Although the NJ tree was usually the same as the ME tree, when the number of taxa was small the difference between the NJ and ME trees can be substantial [20]. In this case if a long DNA or amino acid sequence was used, the ME tree was preferable. When the number of nucleotides or amino acids used was relatively small, the NJ method generated the correct topology more often than did the ME method [21,22]. In this study, the average amino acid-length of 289 GRAS proteins was ~580, so the ME tree was credible. Taken together, the NJ phylogenetic tree was adopted for further analysis. Based on the information from previous analyses and from the topology of the tree and position of conserved motifs, we grouped all the GRAS genes into seven major clusters, group I–VII [7,18]. Group V was further divided into two subgroups, Va and Vb. The numbers of GRAS proteins in different groups were shown in Additional file 1. Among the groups, group II constituted the largest clade. It contained 67 members and accounted for 23.2% of the total GRAS genes. Meanwhile, the number of group II genes from angiosperm also reached the maximum in comparison with the other subgroups, which strongly indicates that these GRAS genes were more likely to be retained in group II. On the contrary, the members of S. moellendorffii and P. patens more gathered in group V. Moreover, the identified DELLA proteins: GAI, RGA, RGL1, RGL2, RGL3, and SLR1 (LOC_Os03g49990) were all present in group IV [8,18]. We also deduced twelve DELLA proteins (Bradi1g11090, Glyma10g33380, Glyma08g10140, Glyma06g23940, Glyma04g21340, Glyma05g27190, Glyma11g33720, Glyma18g04500, 139506, 122441, Pp1s12_244V6, and Pp1s175_16V6) on the basis of the feature that DELLA proteins contain conserved DELLA and VHYNP motifs in their N-terminal regions and belong to group IV. Moreover, the tree (Figure 1) also showed many putative orthologs (e.g., Bradi4g03867/LOC_Os12g38490, Bradi4g43680/LOC_Os03g48450) supported by the high bootstrap values.Figure 1


Unusual tandem expansion and positive selection in subgroups of the plant GRAS transcription factor superfamily.

Wu N, Zhu Y, Song W, Li Y, Yan Y, Hu Y - BMC Plant Biol. (2014)

Phylogenetic tree of GRAS proteins amongArabidopsis,Brachypodium distachyon, rice, soybean,Physcomitrella patens, andSelaginella moellendorffii. A) The major clusters of orthologous genes are shown in different colors: group I = purple, group II = dark blue, group III = yellow, group IV = light green, group V = pink, group VI = dark green, and group VII = light blue. The scale bar corresponds to 0.1 estimated amino acid substitutions per site; B) Genes belonging to the different groups are shown. Among them, the deduced DELLA proteins are indicated by a filled red square, and genes with similar functions clustered together are indicated by filled green circles.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4279901&req=5

Fig1: Phylogenetic tree of GRAS proteins amongArabidopsis,Brachypodium distachyon, rice, soybean,Physcomitrella patens, andSelaginella moellendorffii. A) The major clusters of orthologous genes are shown in different colors: group I = purple, group II = dark blue, group III = yellow, group IV = light green, group V = pink, group VI = dark green, and group VII = light blue. The scale bar corresponds to 0.1 estimated amino acid substitutions per site; B) Genes belonging to the different groups are shown. Among them, the deduced DELLA proteins are indicated by a filled red square, and genes with similar functions clustered together are indicated by filled green circles.
Mentions: Comparison of conserved motifs among members of the GRAS family implied that they can be divided into different groups and subgroups. To better separate the groups and investigate the evolutionary relationships among GRAS proteins in Arabidopsis, B. distachyon, rice, soybean, S. moellendorffii, and P. patens, an unrooted phylogenetic tree was constructed from 289 full-length amino acid sequences using the neighbor-joining (NJ) algorithm (Figure 1 and Additional file 10). To confirm the tree topologies, a ML (maximum likelihood) phylogenetic tree was also constructed, and it showed similar topology to the NJ tree with only minor modifications (Additional file 11). A ME (Minimum-Evolution) phylogenetic tree was also constructed, which showed the same topology to the NJ tree (Additional file 12). Although the NJ tree was usually the same as the ME tree, when the number of taxa was small the difference between the NJ and ME trees can be substantial [20]. In this case if a long DNA or amino acid sequence was used, the ME tree was preferable. When the number of nucleotides or amino acids used was relatively small, the NJ method generated the correct topology more often than did the ME method [21,22]. In this study, the average amino acid-length of 289 GRAS proteins was ~580, so the ME tree was credible. Taken together, the NJ phylogenetic tree was adopted for further analysis. Based on the information from previous analyses and from the topology of the tree and position of conserved motifs, we grouped all the GRAS genes into seven major clusters, group I–VII [7,18]. Group V was further divided into two subgroups, Va and Vb. The numbers of GRAS proteins in different groups were shown in Additional file 1. Among the groups, group II constituted the largest clade. It contained 67 members and accounted for 23.2% of the total GRAS genes. Meanwhile, the number of group II genes from angiosperm also reached the maximum in comparison with the other subgroups, which strongly indicates that these GRAS genes were more likely to be retained in group II. On the contrary, the members of S. moellendorffii and P. patens more gathered in group V. Moreover, the identified DELLA proteins: GAI, RGA, RGL1, RGL2, RGL3, and SLR1 (LOC_Os03g49990) were all present in group IV [8,18]. We also deduced twelve DELLA proteins (Bradi1g11090, Glyma10g33380, Glyma08g10140, Glyma06g23940, Glyma04g21340, Glyma05g27190, Glyma11g33720, Glyma18g04500, 139506, 122441, Pp1s12_244V6, and Pp1s175_16V6) on the basis of the feature that DELLA proteins contain conserved DELLA and VHYNP motifs in their N-terminal regions and belong to group IV. Moreover, the tree (Figure 1) also showed many putative orthologs (e.g., Bradi4g03867/LOC_Os12g38490, Bradi4g43680/LOC_Os03g48450) supported by the high bootstrap values.Figure 1

Bottom Line: All of tandem duplicated genes were found in group II except one cluster of rice, indicating that tandem duplication greatly promoted the expansion of group II.These results strongly indicated that these groups were experiencing higher positive selection pressure.In short, the results above provide a solid foundation for further functional dissection of the GRAS gene superfamily.

View Article: PubMed Central - PubMed

ABSTRACT

Background: GRAS proteins belong to a plant transcription factor family that is involved with multifarious roles in plants. Although previous studies of this protein family have been reported for Arabidopsis, rice, Chinese cabbage and other species, investigation of expansion patterns and evolutionary rate on the basis of comparative genomics in different species remains inadequate.

Results: A total of 289 GRAS genes were identified in Arabidopsis, B. distachyon, rice, soybean, S. moellendorffii, and P. patens and were grouped into seven subfamilies, supported by the similarity of their exon-intron patterns and structural motifs. All of tandem duplicated genes were found in group II except one cluster of rice, indicating that tandem duplication greatly promoted the expansion of group II. Furthermore, segment duplications were mainly found in the soybean genome, whereas no single expansion pattern dominated in other plant species indicating that GRAS genes from these five species might be subject to a more complex evolutionary mechanism. Interestingly, branch-site model analyses of positive selection showed that a number of sites were positively selected under foreground branches I and V. These results strongly indicated that these groups were experiencing higher positive selection pressure. Meanwhile, the site-specific model revealed that the GRAS genes were under strong positive selection in P. patens. DIVERGE v2.0 was used to detect critical amino acid sites, and the results showed that the shifted evolutionary rate was mainly attributed to the functional divergence between the GRAS genes in the two groups. In addition, the results also demonstrated the expression divergence of the GRAS duplicated genes in the evolution. In short, the results above provide a solid foundation for further functional dissection of the GRAS gene superfamily.

Conclusions: In this work, differential expression, evolutionary rate, and expansion patterns of the GRAS gene family in the six species were predicted. Especially, tandem duplication events played an important role in expansion of group II. Together, these results contribute to further functional analysis and the molecular evolution of the GRAS gene superfamily.

Show MeSH
Related in: MedlinePlus