Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection

ABSTRACT The presence of CpG and UpA dinucleotides is restricted in the genomes of animal RNA viruses to avoid specific host defenses. We wondered whether a similar phenomenon exists in nonanimal RNA viruses. Here, we show that these two dinucleotides, especially UpA, are underrepresented in the fam...

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Autores principales:	Alfonso González de Prádena, Adrián Sánchez Jimenez, David San León, Peter Simmonds, Juan Antonio García, Adrián A. Valli
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Potyviridae potyvirus RNA degradation RNA virus antiviral plant defense Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/599322be8cb14b98a7484a8880f4344f
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spelling	oai:doaj.org-article:599322be8cb14b98a7484a8880f4344f2021-11-15T15:56:58ZPlant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection10.1128/mBio.02818-192150-7511https://doaj.org/article/599322be8cb14b98a7484a8880f4344f2020-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02818-19https://doaj.org/toc/2150-7511ABSTRACT The presence of CpG and UpA dinucleotides is restricted in the genomes of animal RNA viruses to avoid specific host defenses. We wondered whether a similar phenomenon exists in nonanimal RNA viruses. Here, we show that these two dinucleotides, especially UpA, are underrepresented in the family Potyviridae, the most important group of plant RNA viruses. Using plum pox virus (PPV; Potyviridae family) as a model, we show that an increase in UpA frequency strongly diminishes virus accumulation. Remarkably, unlike previous observations in animal viruses, PPV variants harboring CpG-rich fragments display just faint (or no) attenuation. The anticorrelation between UpA frequency and viral fitness additionally demonstrates the relevance of this particular dinucleotide: UpA-high mutants are attenuated in a dose-dependent manner, whereas a UpA-low variant displays better fitness than its parental control. Using high-throughput sequencing, we also show that UpA-rich PPV variants are genetically stable, without apparent changes in sequence that revert and/or compensate for the dinucleotide modification despite its attenuation. In addition, we also demonstrate here that the PPV restriction of UpA-rich variants works independently of the classical RNA silencing pathway. Finally, we show that the anticorrelation between UpA frequency and RNA accumulation applies to mRNA-like fragments produced by the host RNA polymerase II. Together, our results inform us about a dinucleotide-based system in plant cells that controls diverse RNAs, including RNA viruses. IMPORTANCE Dinucleotides (combinations of two consecutive nucleotides) are not randomly present in RNA viruses; in fact, the presence of CpG and UpA is significantly repressed in their genomes. Although the meaning of this phenomenon remains obscure, recent studies with animal-infecting viruses have revealed that their low CpG/UpA frequency prevents virus restriction via a host antiviral system that recognizes, and promotes the degradation of, CpG/UpA-rich RNAs. Whether similar systems act in organisms from other life kingdoms has been unknown. To fill this gap in our knowledge, we built several synthetic variants of a plant RNA virus with deoptimized dinucleotide frequencies and analyzed their viral fitness and genome adaptation. In brief, our results inform us for the first time about an effective dinucleotide-based system that acts in plants against viruses. Remarkably, this viral restriction in plants is reminiscent of, but not identical to, the equivalent antiviral response in animals.Alfonso González de PrádenaAdrián Sánchez JimenezDavid San LeónPeter SimmondsJuan Antonio GarcíaAdrián A. ValliAmerican Society for MicrobiologyarticlePotyviridaepotyvirusRNA degradationRNA virusantiviralplant defenseMicrobiologyQR1-502ENmBio, Vol 11, Iss 1 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Potyviridae potyvirus RNA degradation RNA virus antiviral plant defense Microbiology QR1-502
spellingShingle	Potyviridae potyvirus RNA degradation RNA virus antiviral plant defense Microbiology QR1-502 Alfonso González de Prádena Adrián Sánchez Jimenez David San León Peter Simmonds Juan Antonio García Adrián A. Valli Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
description	ABSTRACT The presence of CpG and UpA dinucleotides is restricted in the genomes of animal RNA viruses to avoid specific host defenses. We wondered whether a similar phenomenon exists in nonanimal RNA viruses. Here, we show that these two dinucleotides, especially UpA, are underrepresented in the family Potyviridae, the most important group of plant RNA viruses. Using plum pox virus (PPV; Potyviridae family) as a model, we show that an increase in UpA frequency strongly diminishes virus accumulation. Remarkably, unlike previous observations in animal viruses, PPV variants harboring CpG-rich fragments display just faint (or no) attenuation. The anticorrelation between UpA frequency and viral fitness additionally demonstrates the relevance of this particular dinucleotide: UpA-high mutants are attenuated in a dose-dependent manner, whereas a UpA-low variant displays better fitness than its parental control. Using high-throughput sequencing, we also show that UpA-rich PPV variants are genetically stable, without apparent changes in sequence that revert and/or compensate for the dinucleotide modification despite its attenuation. In addition, we also demonstrate here that the PPV restriction of UpA-rich variants works independently of the classical RNA silencing pathway. Finally, we show that the anticorrelation between UpA frequency and RNA accumulation applies to mRNA-like fragments produced by the host RNA polymerase II. Together, our results inform us about a dinucleotide-based system in plant cells that controls diverse RNAs, including RNA viruses. IMPORTANCE Dinucleotides (combinations of two consecutive nucleotides) are not randomly present in RNA viruses; in fact, the presence of CpG and UpA is significantly repressed in their genomes. Although the meaning of this phenomenon remains obscure, recent studies with animal-infecting viruses have revealed that their low CpG/UpA frequency prevents virus restriction via a host antiviral system that recognizes, and promotes the degradation of, CpG/UpA-rich RNAs. Whether similar systems act in organisms from other life kingdoms has been unknown. To fill this gap in our knowledge, we built several synthetic variants of a plant RNA virus with deoptimized dinucleotide frequencies and analyzed their viral fitness and genome adaptation. In brief, our results inform us for the first time about an effective dinucleotide-based system that acts in plants against viruses. Remarkably, this viral restriction in plants is reminiscent of, but not identical to, the equivalent antiviral response in animals.
format	article
author	Alfonso González de Prádena Adrián Sánchez Jimenez David San León Peter Simmonds Juan Antonio García Adrián A. Valli
author_facet	Alfonso González de Prádena Adrián Sánchez Jimenez David San León Peter Simmonds Juan Antonio García Adrián A. Valli
author_sort	Alfonso González de Prádena
title	Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
title_short	Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
title_full	Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
title_fullStr	Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
title_full_unstemmed	Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection
title_sort	plant virus genome is shaped by specific dinucleotide restrictions that influence viral infection
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/599322be8cb14b98a7484a8880f4344f
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Plant Virus Genome Is Shaped by Specific Dinucleotide Restrictions That Influence Viral Infection

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