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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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Relative evolutionary rate for each site across four plant AGOs classes. (A) shows site specific relative evolutionary rates of AGOs across classes I-IV. Position-by-position (maximum likelihood) relative evolutionary rates are estimated under the JTT amino acid substitution model. Mean (relative) evolutionary rates are scaled such that the average evolutionary rate across all sites is 1. X-axis represent the positions of residues (620 residues) of the ‘AGO dataset II’ along the N-terminal, PAZ, MID and PIWI domains in AGO sequence. Y-axis shows the relative evolutionary rate. Sites showing rates <1 are evolving slower than average and those with rates >1 are evolving faster than average. (B) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a are modeled as representatives of Classes I-IV respectively, and relative evolutionary rates are mapped on to these structures. Sites with green color represent slow evolving sites (rates <1) and those with red color represent fast evolving sites (rates >1). Different colors in the color bar represent the different rate values.
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Fig5: Relative evolutionary rate for each site across four plant AGOs classes. (A) shows site specific relative evolutionary rates of AGOs across classes I-IV. Position-by-position (maximum likelihood) relative evolutionary rates are estimated under the JTT amino acid substitution model. Mean (relative) evolutionary rates are scaled such that the average evolutionary rate across all sites is 1. X-axis represent the positions of residues (620 residues) of the ‘AGO dataset II’ along the N-terminal, PAZ, MID and PIWI domains in AGO sequence. Y-axis shows the relative evolutionary rate. Sites showing rates <1 are evolving slower than average and those with rates >1 are evolving faster than average. (B) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a are modeled as representatives of Classes I-IV respectively, and relative evolutionary rates are mapped on to these structures. Sites with green color represent slow evolving sites (rates <1) and those with red color represent fast evolving sites (rates >1). Different colors in the color bar represent the different rate values.

Mentions: We next determined the 'position-by-position' ML-based relative evolutionary rates using a gamma (γ)-distribution based best substitution model. Of the total 620 sites in ‘AGO dataset II’ (Figure 1, Additional files 2 and 10), 218 sites have a relative rate <1 whereas 69 sites have relative rates >1 in all four classes (Additional file 10: Table S3A). Relatively small ML values of γ- shape parameter were observed for Class I (0.5881; Additional file 10: Table S3B), indicating that the majority of sites (405) in Class I AGOs (Additional file 10: Table S3B) are evolving at slow relative rates. These sites are more frequently found in the MID and PIWI domains (Figure 5). On the other hand, Class III AGOs show a large ML value of the γ- shape parameter (1.0174; Additional file 10: Table S3B), indicating that less number of sites (361 as compared to 405 for example in Class I) are evolving at slow relative rates (Figure 5, Additional file 10: Table S3B).Figure 5


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

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

Relative evolutionary rate for each site across four plant AGOs classes. (A) shows site specific relative evolutionary rates of AGOs across classes I-IV. Position-by-position (maximum likelihood) relative evolutionary rates are estimated under the JTT amino acid substitution model. Mean (relative) evolutionary rates are scaled such that the average evolutionary rate across all sites is 1. X-axis represent the positions of residues (620 residues) of the ‘AGO dataset II’ along the N-terminal, PAZ, MID and PIWI domains in AGO sequence. Y-axis shows the relative evolutionary rate. Sites showing rates <1 are evolving slower than average and those with rates >1 are evolving faster than average. (B) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a are modeled as representatives of Classes I-IV respectively, and relative evolutionary rates are mapped on to these structures. Sites with green color represent slow evolving sites (rates <1) and those with red color represent fast evolving sites (rates >1). Different colors in the color bar represent the different rate values.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Relative evolutionary rate for each site across four plant AGOs classes. (A) shows site specific relative evolutionary rates of AGOs across classes I-IV. Position-by-position (maximum likelihood) relative evolutionary rates are estimated under the JTT amino acid substitution model. Mean (relative) evolutionary rates are scaled such that the average evolutionary rate across all sites is 1. X-axis represent the positions of residues (620 residues) of the ‘AGO dataset II’ along the N-terminal, PAZ, MID and PIWI domains in AGO sequence. Y-axis shows the relative evolutionary rate. Sites showing rates <1 are evolving slower than average and those with rates >1 are evolving faster than average. (B) Threaded structures of NaAGO1a, NaAGO5, NaAGO2 and NaAGO4a are modeled as representatives of Classes I-IV respectively, and relative evolutionary rates are mapped on to these structures. Sites with green color represent slow evolving sites (rates <1) and those with red color represent fast evolving sites (rates >1). Different colors in the color bar represent the different rate values.
Mentions: We next determined the 'position-by-position' ML-based relative evolutionary rates using a gamma (γ)-distribution based best substitution model. Of the total 620 sites in ‘AGO dataset II’ (Figure 1, Additional files 2 and 10), 218 sites have a relative rate <1 whereas 69 sites have relative rates >1 in all four classes (Additional file 10: Table S3A). Relatively small ML values of γ- shape parameter were observed for Class I (0.5881; Additional file 10: Table S3B), indicating that the majority of sites (405) in Class I AGOs (Additional file 10: Table S3B) are evolving at slow relative rates. These sites are more frequently found in the MID and PIWI domains (Figure 5). On the other hand, Class III AGOs show a large ML value of the γ- shape parameter (1.0174; Additional file 10: Table S3B), indicating that less number of sites (361 as compared to 405 for example in Class I) are evolving at slow relative rates (Figure 5, Additional file 10: Table S3B).Figure 5

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