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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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Summary of sequential steps adapted to study evolution of AGOs in plants. A total of 263 AGO sequences from 37 plant species were used in this analysis. Additionally, 5 AGOs from T. castaneum, and 1 each from Human (PDB code 4F3T) and K. polysporus (PDB code 4F1N) were also used (as out groups) to create the ‘AGO dataset I’, comprising a total of 270 AGO sequences. The list of AGOs for each species is available in Additional file 1. After MSA and trimming of poorly aligned regions or large gaps, ‘AGO dataset II’ was generated to contain 270 sequences (rows) and 620 positions (columns; Additional file 2).
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Fig1: Summary of sequential steps adapted to study evolution of AGOs in plants. A total of 263 AGO sequences from 37 plant species were used in this analysis. Additionally, 5 AGOs from T. castaneum, and 1 each from Human (PDB code 4F3T) and K. polysporus (PDB code 4F1N) were also used (as out groups) to create the ‘AGO dataset I’, comprising a total of 270 AGO sequences. The list of AGOs for each species is available in Additional file 1. After MSA and trimming of poorly aligned regions or large gaps, ‘AGO dataset II’ was generated to contain 270 sequences (rows) and 620 positions (columns; Additional file 2).

Mentions: Other than in Arabidopsis, AGOs have been reported in other plant species such as rice, maize, and tomato. These genes, however, have yet been identified in the ecological model plant Nicotiana attenuata in which the smRNA machinery is known to mediate important ecological traits such as herbivore resistance, competitive ability and UV-B tolerance [28-32]. Here, we identify the AGO family of genes in N. attenuata (NaAGO), a plant that grows in agricultural primordial niches and is an important model system for the study of plant-herbivore interactions. Further, we investigated the occurrence of AGO proteins in 17 plant species to identify 133 new AGO proteins in plants. Using integrative biology approach (Figure 1) involving molecular phylogenies, consensus sequence comparisons, signature determination, substitution rate estimations and divergence analysis, we propose a model for the evolutionary history of the AGO family of proteins in plants.Figure 1


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

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

Summary of sequential steps adapted to study evolution of AGOs in plants. A total of 263 AGO sequences from 37 plant species were used in this analysis. Additionally, 5 AGOs from T. castaneum, and 1 each from Human (PDB code 4F3T) and K. polysporus (PDB code 4F1N) were also used (as out groups) to create the ‘AGO dataset I’, comprising a total of 270 AGO sequences. The list of AGOs for each species is available in Additional file 1. After MSA and trimming of poorly aligned regions or large gaps, ‘AGO dataset II’ was generated to contain 270 sequences (rows) and 620 positions (columns; Additional file 2).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Summary of sequential steps adapted to study evolution of AGOs in plants. A total of 263 AGO sequences from 37 plant species were used in this analysis. Additionally, 5 AGOs from T. castaneum, and 1 each from Human (PDB code 4F3T) and K. polysporus (PDB code 4F1N) were also used (as out groups) to create the ‘AGO dataset I’, comprising a total of 270 AGO sequences. The list of AGOs for each species is available in Additional file 1. After MSA and trimming of poorly aligned regions or large gaps, ‘AGO dataset II’ was generated to contain 270 sequences (rows) and 620 positions (columns; Additional file 2).
Mentions: Other than in Arabidopsis, AGOs have been reported in other plant species such as rice, maize, and tomato. These genes, however, have yet been identified in the ecological model plant Nicotiana attenuata in which the smRNA machinery is known to mediate important ecological traits such as herbivore resistance, competitive ability and UV-B tolerance [28-32]. Here, we identify the AGO family of genes in N. attenuata (NaAGO), a plant that grows in agricultural primordial niches and is an important model system for the study of plant-herbivore interactions. Further, we investigated the occurrence of AGO proteins in 17 plant species to identify 133 new AGO proteins in plants. Using integrative biology approach (Figure 1) involving molecular phylogenies, consensus sequence comparisons, signature determination, substitution rate estimations and divergence analysis, we propose a model for the evolutionary history of the AGO family of proteins in plants.Figure 1

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