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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.

Show MeSH
Expansion of AGOs during plant evolution. AGO gene family tree was reconciled with the completely sequenced species tree to identify gain and loss events in each lineage during evolution. The proportions of gains (numerators) versus losses events (denominators) for AGO genes are shown on each of the branches. Lower panel indicates the tentative time of appearance of different members of the AGO family in plants.
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Fig3: Expansion of AGOs during plant evolution. AGO gene family tree was reconciled with the completely sequenced species tree to identify gain and loss events in each lineage during evolution. The proportions of gains (numerators) versus losses events (denominators) for AGO genes are shown on each of the branches. Lower panel indicates the tentative time of appearance of different members of the AGO family in plants.

Mentions: From the analysis of AGO gene expansion and loss (detailed in method section), it was observed that AGOs might have undergone between 133-143 duplication and 272-299 loss events (Figure 3, Additional file 4). We altered the alignment and alignment processing parameters to test the robustness of our analysis. When L-INSI in MAFFT and ‘Automated I’ in TrimAl were used, 140 duplication and 299 loss events were obtained; when the parameters were changed to L-INSI (MAFFT) and user defined parameters in TrimAl (detailed in methods section), 133 duplication and 294 loss events were recorded. Similarly, when Auto options were used for both MAFFT and TrimAl, 143 and 294 duplication and loss events were recorded respectively, whereas 137 duplication and 279 loss events were recorded when ‘Auto’ option in MAFFT and user-defined parameters for TrimAl were used. The reconciliation of species tree and AGO gene family tree (GFT) revealed that the AGO ancestor underwent at least five major duplication events early in its evolution, after the divergence of unicellular green algae, such as, Chlamydomonas and Volvox, but before the divergence of the Bryophytes. This probably gave rise to four distinct phylogenetic clades of AGOs (with strong statistical support with bootstrap values >90%; Figure 2, Additional file 3).Figure 3


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

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

Expansion of AGOs during plant evolution. AGO gene family tree was reconciled with the completely sequenced species tree to identify gain and loss events in each lineage during evolution. The proportions of gains (numerators) versus losses events (denominators) for AGO genes are shown on each of the branches. Lower panel indicates the tentative time of appearance of different members of the AGO family in plants.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: Expansion of AGOs during plant evolution. AGO gene family tree was reconciled with the completely sequenced species tree to identify gain and loss events in each lineage during evolution. The proportions of gains (numerators) versus losses events (denominators) for AGO genes are shown on each of the branches. Lower panel indicates the tentative time of appearance of different members of the AGO family in plants.
Mentions: From the analysis of AGO gene expansion and loss (detailed in method section), it was observed that AGOs might have undergone between 133-143 duplication and 272-299 loss events (Figure 3, Additional file 4). We altered the alignment and alignment processing parameters to test the robustness of our analysis. When L-INSI in MAFFT and ‘Automated I’ in TrimAl were used, 140 duplication and 299 loss events were obtained; when the parameters were changed to L-INSI (MAFFT) and user defined parameters in TrimAl (detailed in methods section), 133 duplication and 294 loss events were recorded. Similarly, when Auto options were used for both MAFFT and TrimAl, 143 and 294 duplication and loss events were recorded respectively, whereas 137 duplication and 279 loss events were recorded when ‘Auto’ option in MAFFT and user-defined parameters for TrimAl were used. The reconciliation of species tree and AGO gene family tree (GFT) revealed that the AGO ancestor underwent at least five major duplication events early in its evolution, after the divergence of unicellular green algae, such as, Chlamydomonas and Volvox, but before the divergence of the Bryophytes. This probably gave rise to four distinct phylogenetic clades of AGOs (with strong statistical support with bootstrap values >90%; Figure 2, Additional file 3).Figure 3

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