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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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Neighbor joining (NJ) based phylogenetic analysis of AGOs. MEGA 5.2 was used to run the NJ analyses. 39 non-plant AGOs were used to determine the root. Clade robustness was assessed with 100 bootstrap replicates.
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Fig2: Neighbor joining (NJ) based phylogenetic analysis of AGOs. MEGA 5.2 was used to run the NJ analyses. 39 non-plant AGOs were used to determine the root. Clade robustness was assessed with 100 bootstrap replicates.

Mentions: During evolution, AGO genes have formed an expanding family across different lineages [1,7]. To determine the evolutionary relatedness of plant AGOs, we reconstructed their phylogeny to evaluate their evolutionary patterns (Figure 1). In order to increase the confidence in the root we included 39 non-plant AGO sequences in the phylogenetic analysis. Plant AGO family proved monophyletic and the phylogenetic tree continued to consist of four major classes/clades (Figure 2, Additional files 1). Both the Neighbor Joining (NJ) and the Maximum Likelihood (ML) approaches were used to reconstruct the phylogeny of plant AGOs and both produced similar tree topologies and phylogenetic distributions into four classes/clades (Additional file 3). Homologs of AGO1 and AGO10 were clustered together (Clade I); similarly homologs of AGOs 2, 3 and 7 formed a clade (Clade III). Likewise, homologs of AGOs 4, 6, 8 and 9 formed the largest cluster (Clade IV), whereas AGO5 homologs formed an independent group (Clade II; Figure 2).Figure 2


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

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

Neighbor joining (NJ) based phylogenetic analysis of AGOs. MEGA 5.2 was used to run the NJ analyses. 39 non-plant AGOs were used to determine the root. Clade robustness was assessed with 100 bootstrap replicates.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig2: Neighbor joining (NJ) based phylogenetic analysis of AGOs. MEGA 5.2 was used to run the NJ analyses. 39 non-plant AGOs were used to determine the root. Clade robustness was assessed with 100 bootstrap replicates.
Mentions: During evolution, AGO genes have formed an expanding family across different lineages [1,7]. To determine the evolutionary relatedness of plant AGOs, we reconstructed their phylogeny to evaluate their evolutionary patterns (Figure 1). In order to increase the confidence in the root we included 39 non-plant AGO sequences in the phylogenetic analysis. Plant AGO family proved monophyletic and the phylogenetic tree continued to consist of four major classes/clades (Figure 2, Additional files 1). Both the Neighbor Joining (NJ) and the Maximum Likelihood (ML) approaches were used to reconstruct the phylogeny of plant AGOs and both produced similar tree topologies and phylogenetic distributions into four classes/clades (Additional file 3). Homologs of AGO1 and AGO10 were clustered together (Clade I); similarly homologs of AGOs 2, 3 and 7 formed a clade (Clade III). Likewise, homologs of AGOs 4, 6, 8 and 9 formed the largest cluster (Clade IV), whereas AGO5 homologs formed an independent group (Clade II; Figure 2).Figure 2

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