Deficiency of the eIF4E isoform nCBP limits the cell-to-cell movement of a plant virus encoding triple-gene-block proteins in Arabidopsis thaliana

Keima, Takuya; Hagiwara‐Komoda, Yuka; Hashimoto, Masayoshi; Neriya, Yutaro; Koinuma, Hiroaki; Iwabuchi, Nozomu; Nishida, Shuko; Yamaji, Yutaka; Namba, Susumu

doi:10.1038/srep39678

Cited by 27 publications

(30 citation statements)

References 58 publications

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“…There are many potential barriers to compatible interactions between plants and viruses. However, our findings are consistent with studies showing that Arabidopsis encodes the necessary components to support Potexvirus replication Hashimoto et al, 2016;Keima et al, 2017) and that abrogation of the RNA silencing machinery is sufficient to render Col-0 an effective host for PVX Yamaji et al, 2012;Andika et al, 2015;Brosseau & Moffett, 2015). Combined with our findings that differential effectiveness of versions of ARGONAUTE2 (AGO2) from different species and accessions, this suggests that natural variation in RNA silencing components may play important roles in host range determination and in ecological dynamics of plant-virus interactions.…”

Section: Susceptibility To Potato Virus X (Pvx) Is Common In a Thalianasupporting

confidence: 91%

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: Susceptibility To Potato Virus X (Pvx) Is Common In a Thalianasupporting

confidence: 91%

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

et al. 2020

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“…There are many potential barriers to compatible interactions between plants and viruses. However, our findings are consistent with studies showing that Arabidopsis encodes the necessary components to support Potexvirus replication 8,28,29 and that abrogation of the RNA silencing machinery is sufficient to render Col-0 an effective host for PVX 8,15,19,30 . Combined with our findings that differential effectiveness of versions of AGO2 from different species and accessions, this suggests that natural variation in RNA silencing components may play important roles in host range determination and in ecological dynamics of plant-virus interactions.…”

Section: Discussionsupporting

confidence: 91%

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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“…There is no precedent for recruitment of nCBPs by potyviral VPg proteins. However, nCBP has been identified as a novel recessive resistance gene towards viruses in the Alphaflexiviridae and Betaflexiviridae families, specifically by inhibiting accumulation of movement proteins from a viral subgenomic RNA (Keima et al, 2017). nCBP may be similarly involved in the accumulation of the CBSV movement protein, although differences in viral replication strategies suggest a different underlying mechanism (Hagiwara-Komoda et al, 2016; Olspert et al, 2015;Rodamilans et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Simultaneous CRISPR/Cas9‐mediated editing of cassava eIF4E isoforms nCBP‐1 and nCBP‐2 reduces cassava brown streak disease symptom severity and incidence

Gomez

Lin

Moll

et al. 2018

Plant Biotechnology Journal

268

148

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Cassava brown streak disease (CBSD) is a major constraint on cassava yields in East and Central Africa and threatens production in West Africa. CBSD is caused by two species of positive-sense RNA viruses belonging to the family Potyviridae, genus Ipomovirus: Cassava brown streak virus (CBSV) and Ugandan cassava brown streak virus (UCBSV). Diseases caused by the family Potyviridae require the interaction of viral genome-linked protein (VPg) and host eukaryotic translation initiation factor 4E (eIF4E) isoforms. Cassava encodes five eIF4E proteins: eIF4E, eIF(iso)4E-1, eIF(iso)4E-2, novel cap-binding protein-1 (nCBP-1), and nCBP-2. Protein-protein interaction experiments consistently found that VPg proteins associate with cassava nCBPs. CRISPR/Cas9-mediated genome editing was employed to generate ncbp-1, ncbp-2, and ncbp-1/ncbp-2 mutants in cassava cultivar 60444. Challenge with CBSV showed that ncbp-1/ncbp-2 mutants displayed delayed and attenuated CBSD aerial symptoms, as well as reduced severity and incidence of storage root necrosis. Suppressed disease symptoms were correlated with reduced virus titre in storage roots relative to wild-type controls. Our results demonstrate the ability to modify multiple genes simultaneously in cassava to achieve tolerance to CBSD. Future studies will investigate the contribution of remaining eIF4E isoforms on CBSD and translate this knowledge into an optimized strategy for protecting cassava from disease.

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Deficiency of the eIF4E isoform nCBP limits the cell-to-cell movement of a plant virus encoding triple-gene-block proteins in Arabidopsis thaliana

Cited by 27 publications

References 58 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

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

Simultaneous CRISPR/Cas9‐mediated editing of cassava eIF4E isoforms nCBP‐1 and nCBP‐2 reduces cassava brown streak disease symptom severity and incidence

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