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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 residue bias (probability; lower panel) and relative evolution rate (upper panel) at functionally important positions in the three domains of AGOs in the plant kingdom. Relative frequency of each residue is represented by the height of the corresponding symbol. Height of the bar indicates the relative rate value for respective position. The positions marked with stars (in grey color) are the previously known signature residues.
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Fig4: Relative residue bias (probability; lower panel) and relative evolution rate (upper panel) at functionally important positions in the three domains of AGOs in the plant kingdom. Relative frequency of each residue is represented by the height of the corresponding symbol. Height of the bar indicates the relative rate value for respective position. The positions marked with stars (in grey color) are the previously known signature residues.

Mentions: Phylogenetic analysis indicates the presence of four clades/classes of AGOs and that these have been evolving differently. In addition, in plants, different AGOs are known to interact with different types of smRNAs (as described in the Background), wherein each residue of the 7nt region of smRNA, ‘the seed region’, sits in a narrow groove to interact with different residues of the MID-PIWI lobe of AGO proteins [10]. It is hypothesized that the sorting of different species of smRNAs to various AGOs [22,23] may depend on the conservation of these residues across various AGOs. Such functionally important residues may also be regarded as signatures of specific domains. Therefore, we attempted to define class-wise signature residues for each of the four classes as well as to re-examine the overarching architecture of AGO sequences in plant genomes. The N-terminal domain of AGOs is the most variable domain, whereas, 'R/K-F-Y', 'Y-N-K-K', 'D-E-D-H/D' have been regarded as the signatures of PAZ, MID and PIWI domains, respectively [7]. Upon examining the MSA of all the plant AGOs, we found 55 positions (column score >90) with highly conserved residues (Additional file 2). In parallel, we also examined the MSA of plant AGOs in each of the four classes independently to determine class-wise signature residues (Figure 4). We identified 8 sites in the PAZ domains, 12 sites in the MID domains and 15 sites in the PIWI domains that show conservation in the four classes AGOs. In the MID domain, residues ‘K’, ‘Q’ and ‘C’ (alignment position 2485, 2497 and 2498, respectively), thought to directly bind to the 5’-phosphate of smRNAs [10], are conserved in all four classes (Figure 4). Similarly, ‘K and ‘S’ (alignment position 2834 and 2954) of PIWI domain are conserved in all the four classes (Figure 4).Figure 4


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 residue bias (probability; lower panel) and relative evolution rate (upper panel) at functionally important positions in the three domains of AGOs in the plant kingdom. Relative frequency of each residue is represented by the height of the corresponding symbol. Height of the bar indicates the relative rate value for respective position. The positions marked with stars (in grey color) are the previously known signature residues.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Relative residue bias (probability; lower panel) and relative evolution rate (upper panel) at functionally important positions in the three domains of AGOs in the plant kingdom. Relative frequency of each residue is represented by the height of the corresponding symbol. Height of the bar indicates the relative rate value for respective position. The positions marked with stars (in grey color) are the previously known signature residues.
Mentions: Phylogenetic analysis indicates the presence of four clades/classes of AGOs and that these have been evolving differently. In addition, in plants, different AGOs are known to interact with different types of smRNAs (as described in the Background), wherein each residue of the 7nt region of smRNA, ‘the seed region’, sits in a narrow groove to interact with different residues of the MID-PIWI lobe of AGO proteins [10]. It is hypothesized that the sorting of different species of smRNAs to various AGOs [22,23] may depend on the conservation of these residues across various AGOs. Such functionally important residues may also be regarded as signatures of specific domains. Therefore, we attempted to define class-wise signature residues for each of the four classes as well as to re-examine the overarching architecture of AGO sequences in plant genomes. The N-terminal domain of AGOs is the most variable domain, whereas, 'R/K-F-Y', 'Y-N-K-K', 'D-E-D-H/D' have been regarded as the signatures of PAZ, MID and PIWI domains, respectively [7]. Upon examining the MSA of all the plant AGOs, we found 55 positions (column score >90) with highly conserved residues (Additional file 2). In parallel, we also examined the MSA of plant AGOs in each of the four classes independently to determine class-wise signature residues (Figure 4). We identified 8 sites in the PAZ domains, 12 sites in the MID domains and 15 sites in the PIWI domains that show conservation in the four classes AGOs. In the MID domain, residues ‘K’, ‘Q’ and ‘C’ (alignment position 2485, 2497 and 2498, respectively), thought to directly bind to the 5’-phosphate of smRNAs [10], are conserved in all four classes (Figure 4). Similarly, ‘K and ‘S’ (alignment position 2834 and 2954) of PIWI domain are conserved in all the four classes (Figure 4).Figure 4

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