A Primary Sequence Analysis of the ARGONAUTE Protein Family in Plants

Rodríguez-Leal, Daniel; Castillo-Cobián, Amanda; Rodríguez‐Arévalo, Isaac; Vielle‐Calzada, Jean‐Philippe

doi:10.3389/fpls.2016.01347

Cited by 26 publications

(25 citation statements)

References 53 publications

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“…The most frequent polymorphisms in the AGO2 coding sequence, ΔGR and D33G, are both found in a region of the protein identified as Block 43, (Figs b, ) (Rodríguez‐Leal et al , ). This motif is present in different copy numbers in different AGO proteins from animal and plant species and, although well conserved, its function is unknown (Rodríguez‐Leal et al , ). It is notable that in nearly all cases these two polymorphisms are either both absent or both present (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…A primary sequence analysis of plant AGO proteins has identified the region including the GR repeats and residue 33 as being composed of multiple GR‐rich blocks, known as B43 motifs, which are present in varying copy numbers in AGO1, 2, 3, 5 and 10 (Rodríguez‐Leal et al , ). In numerous animal and plant AGOs, arginine residues within this block have been shown to be methylated by PMRT (Kirino et al , , ; Vagin et al , ; Siomi et al , ; Musiyenko et al , ; Hu et al , ).…”

Section: Discussionmentioning

confidence: 99%

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Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

et al. 2020

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Summary RNA silencing functions as an anti‐viral defence in plants through the action of DICER‐like (DCL) and ARGONAUTE (AGO) proteins. Despite the importance of this mechanism, little is known about the functional consequences of variation in genes encoding RNA silencing components. The AGO2 protein has been shown to be important for defense against multiple viruses, and we investigated how naturally occurring differences in AGO2 between and within species affects its antiviral activities. We find that the AGO2 protein from Arabidopsis thaliana, but not Nicotiana benthamiana, effectively limits potato virus X (PVX). Consistent with this, we find that the A. thaliana AGO2 gene shows a high incidence of polymorphisms between accessions, with evidence of selective pressure. Using functional analyses, we identify polymorphisms that specifically affect AGO2 antiviral activity, without interfering with other AGO2‐associated functions such as anti‐bacterial resistance or DNA methylation. Our results suggest that viruses adapt to overcome RNA silencing in their hosts. Furthermore, they indicate that plant–virus interactions have influenced natural variation in RNA‐silencing components and that the latter may be a source of genetically encoded virus resistance.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

et al. 2020

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“…Once loaded into Argonaute, sRNA guide the silencing machinery to targets through base pairing principles. Argonautes are highly conserved proteins with family members in most eukaryotes (4)(5)(6). Although there are two main subfamilies of Argonautes in eukaryotes: AGO and PIWI; only AGO proteins can be found in plants.…”

Section: Introductionmentioning

confidence: 99%

“…Although there are two main subfamilies of Argonautes in eukaryotes: AGO and PIWI; only AGO proteins can be found in plants. Also in plants, AGOs can be grouped into three phylogenetic clades with a highly variable number of elements from species to species (5) (Fig. 2).…”

Section: Introductionmentioning

confidence: 99%

Learning sequence patterns of AGO-sRNA affinity from high-throughput sequencing libraries to improve in silico functional small RNA detection and classification in plants

Morgado

Jansen

Johannes

2017

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The loading of small RNA (sRNA) into Argonaute (AGO) complexes is a crucial step in all regulatory pathways identified so far in plants that depend on such non-coding sequences. Important transcriptional and post-transcriptional silencing mechanisms can be activated depending on the specific AGO protein to which sRNA bind. It is known that sRNA-AGO associations are at least partly encoded in the sRNA primary structure, but the sequence features that drive this association have not been fully explored. Here we train support vector machines (SVM) on sRNA sequencing data obtained from AGO-immunoprecipitation experiments to identify features that determine sRNA affinity to specific AGOs. Our SVM reveal that AGO affinity is strongly determined by complex k-mers in the 5' and 3' ends of sRNA, in addition to well-known features such as sRNA length and the base composition of the first nucleotide. Moreover, we find that these k-mers tend to overlap known transcription factor (TF) binding motifs, thus highlighting a close interplay between TF and sRNAmediated transcriptional regulation. We embedded the learned SVM in a computational pipeline that can be used for de novo functional classification of sRNA sequences. This tool, called SAILS, is provided as a web portal accessible at http://sails.eu.nu.

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“…3) 43 . This motif is present in different copy numbers in different AGO proteins from animal and plant species and, although well conserved, its function is unknown 43 . It is of notable that in nearly all cases these two polymorphisms are either both absent or both present (Fig.…”

Section: Discussionmentioning

confidence: 99%

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

Brosseau

Adurogbangba

Roussin-Léveillée

et al. 2019

Preprint

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24RNA silencing functions as an anti-viral defence in plants through the action of DICER-like 25 (DCL) and ARGONAUTE (AGO) proteins. However, there are few known examples of 26 functional variation in RNA silencing components. The AGO2 protein is important for antiviral 27 defense against multiple viruses and has been shown to be a major limiting factor to infection 28 by potato virus X (PVX) of Arabidopsis thaliana but not Nicotiana benthamiana. We show that 29 the AGO2 proteins from these two plants have differential activity against PVX, suggesting that 30 variation in AGO2 is important in plant-virus interactions. Consistent with this, we find that the 31 Arabidopsis thaliana AGO2 gene shows a high incidence of polymorphisms between 32 accessions, with evidence of selective pressure. AGO2 protein variants can be assigned to two 33 groups, in near equal frequency, based on an amino acid change and small deletions in the 34 protein N-terminus. Inoculation of a large number of Arabidopsis accessions shows strong 35 correlation between these alleles and resistance or susceptibility to PVX. These observations 36 were validated using genetic and transgenic complementation analysis, which showed that one 37 type of AGO2 variant is specifically affected in its antiviral activity, without interfering with other 38 AGO2-associated functions such as anti-bacterial resistance or DNA methylation. Our results 39 demonstrate a novel type of genetically-encoded virus resistance and suggest that plant-virus 40 interactions have influenced natural variation in RNA silencing components. 41 42 43 44Here, we show that AGO2 proteins from A. thaliana and N. benthamiana manifest 68 differing activities against PVX, suggesting that inter-specific differences in AGO2 may 69 contribute to differing outcomes of PVX infection in these species. Furthermore, we tested 70 whether intra-specific differences in AGO2 might affect plant-virus interactions by taking 71 advantage of the natural genetic variation of wild Arabidopsis accessions. We show the AGO2 72 gene presents a high level of polymorphism and shows evidence of having been subject to 73 selective pressure. Furthermore, unlike the commonly used Arabidopsis accession Col-0, 27 74 out of 63 accessions analysed were found to susceptible to PVX. Through genetic and 75 transgenic analysis, we show that this susceptibility is determined by two polymorphisms found 76 in the N-terminus of the AGO2 protein. Our results have uncovered a novel form of genetically-77 encoded virus resistance. Likewise, it suggests that natural variation in AGO2 may be important 78 for determining plant-virus interaction outcomes and that in turn these pressures may have 79 shaped the RNA silencing machinery in ways similar to other defense mechanisms.80

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A Primary Sequence Analysis of the ARGONAUTE Protein Family in Plants

Cited by 26 publications

References 53 publications

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

Learning sequence patterns of AGO-sRNA affinity from high-throughput sequencing libraries to improve in silico functional small RNA detection and classification in plants

Natural variation in the Arabidopsis AGO2 gene is associated with susceptibility to potato virus X

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