Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses

Zamora, Miguel; Méndez-López, Eduardo; Agirrezabala, Xabier; Cuesta, Rebeca; Lavín, José L.; Sánchez-Pina, M. Amelia; Aranda, Miguel A.; Valle, Mikel

doi:10.1126/sciadv.aao2182

Cited by 67 publications

(100 citation statements)

References 45 publications

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“…The vast majority of the remaining 10-50% are bacterial and archaeal viruses with icosahedral capsids and helical tails (order Caudovirales). Apart from icosahedra, numerous viruses, especially, those infecting plants and archaea, have elongated, rod-shaped or filamentous capsids [64][65][66][67][68] whereas others, such as numerous negative-strand RNA viruses of animals, have helical nucleocapsids [69][70][71] . Finally, there is a long 'tail' of odd-shaped virions such as those found in numerous viruses of hyperthermophilic archaea 72 .…”

Section: [H1] Diversity Of Virus Capsidsmentioning

confidence: 99%

Origin of viruses: primordial replicators recruiting capsids from hosts

2019

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Viruses are ubiquitous parasites of cellular life and the most abundant biological entities on earth. It is widely accepted that viruses are polyphyletic but a consensus scenario for their ultimate origin(s) is still lacking. Traditionally, three different scenarios have been considered for the origin of viruses: descent from primordial, pre-cellular genetic elements, reductive evolution from cellular ancestors, and escape of genes from cellular hosts achieving partial replicative autonomy and becoming parasitic genetic elements. These three classical scenarios give different timelines for the origin of viruses and do not explain the provenance of the two key functional modules that are responsible, respectively, for virus genome replication and virion morphogenesis. Here we outline a 'chimeric' scenario under which different types of primordial, selfish replicons gave rise to viruses by recruiting host proteins for virion formation. We also propose that new groups of viruses have repeatedly emerged at all stages of the evolution of life, often, through the displacement of ancestral structural and genome replication genes. [H1] Introduction Viruses are the most abundant biological entities on our planet and have major roles in global ecology and evolution of the biosphere 1-4. All cellular organisms, with the possible exception of some intracellular parasitic bacteria, harbour distinctive repertoires of viruses, that is, obligate intracellular genetic parasites that package their genomes into virus particles (virions) 5. The ubiquity of viruses, combined with the theoretical argument that genetic parasites will inevitably emerge in replicator systems 6,7 , implies that the entire course of the evolution of life is actually a story of virus-host coevolution 4,8-10. Accordingly, evolution of life cannot be understood without elucidating the origin(s) of viruses, yet, these origins currently remain mysterious. Historically, three distinct scenarios of virus origin have been considered 11-17 (Figure 1). According to the 'primordial virus world' or 'virus early' hypothesis, viruses are direct descendants of the first replicons that existed during the pre-cellular stage of the evolution of life. By contrast, in the 'reductive virus origin' or 'regression' scenario, viruses are the ultimate products of degeneration of ancestral cells that have lost their autonomy and transitioned to obligate intracellular parasitism. Finally, in the 'escaped genes' scenario, viruses evolved on multiple, independent occasions in different cellular organisms from host genes that acquired the capacity for (quasi)autonomous, selfish replication and infectivity. Accordingly, escaped bacterial, archaeal and eukaryotic genes are thought to have given rise to bacterial, 2 archaeal and eukaryotic viruses, respectively. The three scenarios seem to be mutually exclusive with respect to the origin of any particular group of viruses but different groups of viruses potentially could have evolved via different routes. Over the years, all three scenari...

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Section: [H1] Diversity Of Virus Capsidsmentioning

confidence: 99%

Origin of viruses: primordial replicators recruiting capsids from hosts

2019

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“…Likewise, there were significant similarities between the PVY RdRp region and that of astroviruses (see below). Structural studies have only been reported for the CP protein of one potyvirus, watermelon mosaic virus (WMV), and reveal a structure that is closely similar to those of other viruses with flexuous filamentous virions, including two potexviruses, and also the enveloped flexuous nucleoproteins of orthomyxoviruses and bunyavirids, which include tomato spotted wilt tospovirus [19][20][21]; all these CPs have a core domain rich in alpha helices. Each CP subunit interacts with five nucleotides (nts), and has 8.8 subunits per turn in a left-handed helix, with a pitch of 34.5-35 Å.…”

Section: The Origins Of the Potyviridaementioning

confidence: 99%

The Potyviruses: An Evolutionary Synthesis Is Emerging

Gibbs

Hajizadeh

Ohshima

et al. 2020

Viruses

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In this review, encouraged by the dictum of Theodosius Dobzhansky that “Nothing in biology makes sense except in the light of evolution”, we outline the likely evolutionary pathways that have resulted in the observed similarities and differences of the extant molecules, biology, distribution, etc. of the potyvirids and, especially, its largest genus, the potyviruses. The potyvirids are a family of plant-infecting RNA-genome viruses. They had a single polyphyletic origin, and all share at least three of their genes (i.e., the helicase region of their CI protein, the RdRp region of their NIb protein and their coat protein) with other viruses which are otherwise unrelated. Potyvirids fall into 11 genera of which the potyviruses, the largest, include more than 150 distinct viruses found worldwide. The first potyvirus probably originated 15,000–30,000 years ago, in a Eurasian grass host, by acquiring crucial changes to its coat protein and HC-Pro protein, which enabled it to be transmitted by migrating host-seeking aphids. All potyviruses are aphid-borne and, in nature, infect discreet sets of monocotyledonous or eudicotyledonous angiosperms. All potyvirus genomes are under negative selection; the HC-Pro, CP, Nia, and NIb genes are most strongly selected, and the PIPO gene least, but there are overriding virus specific differences; for example, all turnip mosaic virus genes are more strongly conserved than those of potato virus Y. Estimates of dN/dS (ω) indicate whether potyvirus populations have been evolving as one or more subpopulations and could be used to help define species boundaries. Recombinants are common in many potyvirus populations (20%–64% in five examined), but recombination seems to be an uncommon speciation mechanism as, of 149 distinct potyviruses, only two were clear recombinants. Human activities, especially trade and farming, have fostered and spread both potyviruses and their aphid vectors throughout the world, especially over the past five centuries. The world distribution of potyviruses, especially those found on islands, indicates that potyviruses may be more frequently or effectively transmitted by seed than experimental tests suggest. Only two meta-genomic potyviruses have been recorded from animal samples, and both are probably contaminants.

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“…Moreover, RNA polymerase slippage events generate virus-derived RNA variants producing diverse transframe products whose expression varies among potyviruses and include P3N-PIPO, P3N-ALT, and P1N-PISPO (4)(5)(6)(7)(8). The genomic RNA is encapsidated by a single core CP that forms characteristic potyviral flexuous rods of 11 to 20 nm in diameter by 680 to 900 nm in length (2,9). The CP is able to self-assemble in vitro as well as in different heterologous systems (10)(11)(12)(13), and once assembled, the particles remain stable after trimming the surfaceexposed N-and C-terminal regions of CP by a mild trypsin treatment (14,15).…”

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confidence: 99%

A Functional Link between RNA Replication and Virion Assembly in the Potyvirus Plum Pox Virus

Gallo

Vallí

Calvo

et al. 2018

J Virol

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Accurate assembly of viral particles in the potyvirus (PPV) has been shown to depend on the contribution of the multifunctional viral protein HCPro. In this study, we show that other viral factors, in addition to the capsid protein (CP) and HCPro, are necessary for the formation of stable PPV virions. The CP produced in leaves from a subviral RNA termed LONG, which expresses a truncated polyprotein that lacks P1 and HCPro, together with HCPro supplied , was assembled into virus-like particles and remained stable after incubation. In contrast, deletions in multiple regions of the LONG coding sequence prevented the CP stabilization mediated by HCPro. In particular, we demonstrated that the first 178 amino acids of P3, but not a specific nucleotide sequence coding for them, are required for CP stability and proper assembly of PPV particles. Using a sequential coagroinfiltration assay, we observed that the subviral LONG RNA replicates and locally spreads in leaves expressing an RNA silencing suppressor. The analysis of the effect of both point and deletion mutations affecting RNA replication in LONG and full-length PPV demonstrated that this process is essential for the assembly of stable viral particles. Interestingly, in spite of this requirement, the CP produced by a nonreplicating viral RNA can be stably assembled into virions as long as it is coexpressed with a replication-proficient RNA. Altogether, these results highlight the importance of coupling encapsidation to other viral processes to secure a successful infection. Viruses of the family are among the most dangerous threats for basically every important crop, and such socioeconomical relevance has made them a subject of many research studies. In spite of this, very little is currently known about proteins and processes controlling viral genome encapsidation by the coat protein. In the case of (genus ), for instance, we have previously shown that the multitasking viral factor HCPro plays a role in the production of stable virions. Here, by using this potyvirus as a model, we move further to show that additional factors are also necessary for the efficient production of potyviral particles. More importantly, a comprehensive screening for such factors led us to the identification of a functional link between virus replication and packaging, unraveling a previously unknown connection of these two key events of the potyviral infection cycle.

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Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses

Abstract: A widespread common protein fold packages ssRNA in virus particles with diverse morphology and genomic structure.

Cited by 67 publications

References 45 publications

Origin of viruses: primordial replicators recruiting capsids from hosts

Origin of viruses: primordial replicators recruiting capsids from hosts

The Potyviruses: An Evolutionary Synthesis Is Emerging

A Functional Link between RNA Replication and Virion Assembly in the Potyvirus Plum Pox Virus

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