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Molecular evolution and diversification of the Argonaute family of proteins in plants.

Singh RK, Gase K, Baldwin IT, Pandey SP - BMC Plant Biol. (2015)

Bottom Line: Here, we not only identify 11 AGOs in N. attenuata, we further annotate 133 genes in 17 plant species, previously not annotated in the Phytozome database, to increase the number of plant AGOs to 263 genes from 37 plant species.Class-specific signatures in the RNA-binding and catalytic domains, which may contribute to the functional diversity of plant AGOs, as well as context-dependent changes in sequence and domain architecture that may have consequences for gene function were found.Together, the results demonstrate that the evolution of AGOs has been a dynamic process producing the signatures of functional diversification in the smRNA pathways of higher plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Indian Institute of Science Education and Research Kolkata, Mohanpur Campus, Mohanpur, Nadia, 741246, West Bengal, India. rks12rs025@iiserkol.ac.in.

ABSTRACT

Background: Argonaute (AGO) proteins form the core of the RNA-induced silencing complex, a central component of the smRNA machinery. Although reported from several plant species, little is known about their evolution. Moreover, these genes have not yet been cloned from the ecological model plant, Nicotiana attenuata, in which the smRNA machinery is known to mediate important ecological traits.

Results: Here, we not only identify 11 AGOs in N. attenuata, we further annotate 133 genes in 17 plant species, previously not annotated in the Phytozome database, to increase the number of plant AGOs to 263 genes from 37 plant species. We report the phylogenetic classification, expansion, and diversification of AGOs in the plant kingdom, which resulted in the following hypothesis about their evolutionary history: an ancestral AGO underwent duplication events after the divergence of unicellular green algae, giving rise to four major classes with subsequent gains/losses during the radiation of higher plants, resulting in the large number of extant AGOs. Class-specific signatures in the RNA-binding and catalytic domains, which may contribute to the functional diversity of plant AGOs, as well as context-dependent changes in sequence and domain architecture that may have consequences for gene function were found.

Conclusions: Together, the results demonstrate that the evolution of AGOs has been a dynamic process producing the signatures of functional diversification in the smRNA pathways of higher plants.

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Related in: MedlinePlus

CAPS 2.0 analysis of coevolving sites in plant AGOs. (A) shows heatmaps of coevolving sites in the four classes of plant AGOs. Coevolving pairs showing correlation coefficient of ≥0.5 are plotted. (B) is the color-coded representation of the coevolution frequency matrix of 20 amino acid pairs in NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a, the representatives of four classes respectively. (C) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a show the position and arrangement of top coevolving groups in the classes I-IV respectively (orange, green and blue colored; residues in black represent other functionally important coevolving sites as described in Results and Discussion). Residues coded with same color show the correlation with each other in evolutionary context.
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Fig6: CAPS 2.0 analysis of coevolving sites in plant AGOs. (A) shows heatmaps of coevolving sites in the four classes of plant AGOs. Coevolving pairs showing correlation coefficient of ≥0.5 are plotted. (B) is the color-coded representation of the coevolution frequency matrix of 20 amino acid pairs in NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a, the representatives of four classes respectively. (C) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a show the position and arrangement of top coevolving groups in the classes I-IV respectively (orange, green and blue colored; residues in black represent other functionally important coevolving sites as described in Results and Discussion). Residues coded with same color show the correlation with each other in evolutionary context.

Mentions: The evolution of protein residues is frequently context-dependent in that substitutions at a given site are affected by local structure, residues at the other sites, and related functions. Such context-dependent substitutions result in co-evolution of amino-acid residues that have implications for protein structure and function. We uncovered coevolving residues in plant AGOs by using Pearson correlation coefficient (r) as implemented in CAPS 2.0 (coevolution analysis using protein sequences) algorithm [34]. Only co-evolving sites with r ≥ 0.5 were considered significant (Figure 6, Additional file 14: Table S5A). Class III AGOs accounted for largest number of coevolving residues (Figure 6A, Additional file 14: Table S5A). Strong correlation of r > 0.9 was observed between the sites coevolving in the PAZ domain and PIWI domain of Class III AGOs (Figure 6A, Additional file 14: Table S5A). Four classes of AGOs displayed heterogenous coevolving groups of residues that are of different sizes. In Class III AGOs, PIWI domains displayed the largest number of coevolving residues (Figure 6A, Additional file 14: Table S5B). In general, the amino acid residue 'R' is the most frequently correlating residue in Class I and II, while residue ‘L’ is found most frequently correlating in Classes III and IV (Figure 6B, Additional file 14: Table S5C). In Class I, 'G' is the second most frequent residue that is significantly correlated mainly to 'G', 'Q', ‘R’ and 'H'. In Class II, ‘G’ is again the second most frequent residue that instead significantly correlates to 'V', 'S', ‘E’, 'K' and 'R' (Figure 6B, Additional file 14: Table S5C). In Class III and IV, ‘P’ is the second most frequent residue that significantly correlates frequently to ‘V’, ‘Q’ and ‘F’, and to ‘P’, ‘G’ and 'R' respectively (Figure 6B, Additional file 14: Table S5C).Figure 6


Molecular evolution and diversification of the Argonaute family of proteins in plants.

Singh RK, Gase K, Baldwin IT, Pandey SP - BMC Plant Biol. (2015)

CAPS 2.0 analysis of coevolving sites in plant AGOs. (A) shows heatmaps of coevolving sites in the four classes of plant AGOs. Coevolving pairs showing correlation coefficient of ≥0.5 are plotted. (B) is the color-coded representation of the coevolution frequency matrix of 20 amino acid pairs in NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a, the representatives of four classes respectively. (C) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a show the position and arrangement of top coevolving groups in the classes I-IV respectively (orange, green and blue colored; residues in black represent other functionally important coevolving sites as described in Results and Discussion). Residues coded with same color show the correlation with each other in evolutionary context.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4318128&req=5

Fig6: CAPS 2.0 analysis of coevolving sites in plant AGOs. (A) shows heatmaps of coevolving sites in the four classes of plant AGOs. Coevolving pairs showing correlation coefficient of ≥0.5 are plotted. (B) is the color-coded representation of the coevolution frequency matrix of 20 amino acid pairs in NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a, the representatives of four classes respectively. (C) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a show the position and arrangement of top coevolving groups in the classes I-IV respectively (orange, green and blue colored; residues in black represent other functionally important coevolving sites as described in Results and Discussion). Residues coded with same color show the correlation with each other in evolutionary context.
Mentions: The evolution of protein residues is frequently context-dependent in that substitutions at a given site are affected by local structure, residues at the other sites, and related functions. Such context-dependent substitutions result in co-evolution of amino-acid residues that have implications for protein structure and function. We uncovered coevolving residues in plant AGOs by using Pearson correlation coefficient (r) as implemented in CAPS 2.0 (coevolution analysis using protein sequences) algorithm [34]. Only co-evolving sites with r ≥ 0.5 were considered significant (Figure 6, Additional file 14: Table S5A). Class III AGOs accounted for largest number of coevolving residues (Figure 6A, Additional file 14: Table S5A). Strong correlation of r > 0.9 was observed between the sites coevolving in the PAZ domain and PIWI domain of Class III AGOs (Figure 6A, Additional file 14: Table S5A). Four classes of AGOs displayed heterogenous coevolving groups of residues that are of different sizes. In Class III AGOs, PIWI domains displayed the largest number of coevolving residues (Figure 6A, Additional file 14: Table S5B). In general, the amino acid residue 'R' is the most frequently correlating residue in Class I and II, while residue ‘L’ is found most frequently correlating in Classes III and IV (Figure 6B, Additional file 14: Table S5C). In Class I, 'G' is the second most frequent residue that is significantly correlated mainly to 'G', 'Q', ‘R’ and 'H'. In Class II, ‘G’ is again the second most frequent residue that instead significantly correlates to 'V', 'S', ‘E’, 'K' and 'R' (Figure 6B, Additional file 14: Table S5C). In Class III and IV, ‘P’ is the second most frequent residue that significantly correlates frequently to ‘V’, ‘Q’ and ‘F’, and to ‘P’, ‘G’ and 'R' respectively (Figure 6B, Additional file 14: Table S5C).Figure 6

Bottom Line: Here, we not only identify 11 AGOs in N. attenuata, we further annotate 133 genes in 17 plant species, previously not annotated in the Phytozome database, to increase the number of plant AGOs to 263 genes from 37 plant species.Class-specific signatures in the RNA-binding and catalytic domains, which may contribute to the functional diversity of plant AGOs, as well as context-dependent changes in sequence and domain architecture that may have consequences for gene function were found.Together, the results demonstrate that the evolution of AGOs has been a dynamic process producing the signatures of functional diversification in the smRNA pathways of higher plants.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Indian Institute of Science Education and Research Kolkata, Mohanpur Campus, Mohanpur, Nadia, 741246, West Bengal, India. rks12rs025@iiserkol.ac.in.

ABSTRACT

Background: Argonaute (AGO) proteins form the core of the RNA-induced silencing complex, a central component of the smRNA machinery. Although reported from several plant species, little is known about their evolution. Moreover, these genes have not yet been cloned from the ecological model plant, Nicotiana attenuata, in which the smRNA machinery is known to mediate important ecological traits.

Results: Here, we not only identify 11 AGOs in N. attenuata, we further annotate 133 genes in 17 plant species, previously not annotated in the Phytozome database, to increase the number of plant AGOs to 263 genes from 37 plant species. We report the phylogenetic classification, expansion, and diversification of AGOs in the plant kingdom, which resulted in the following hypothesis about their evolutionary history: an ancestral AGO underwent duplication events after the divergence of unicellular green algae, giving rise to four major classes with subsequent gains/losses during the radiation of higher plants, resulting in the large number of extant AGOs. Class-specific signatures in the RNA-binding and catalytic domains, which may contribute to the functional diversity of plant AGOs, as well as context-dependent changes in sequence and domain architecture that may have consequences for gene function were found.

Conclusions: Together, the results demonstrate that the evolution of AGOs has been a dynamic process producing the signatures of functional diversification in the smRNA pathways of higher plants.

Show MeSH
Related in: MedlinePlus