ICTV VIRUS TAXONOMY PROFILE Inoue-­Nagata et al., Journal of General Virology 2022;103:001738 DOI 10.1099/jgv.0.001738 OPEN ICTV ACCESS ICTV Virus Taxonomy Profile: Potyviridae 2022 Alice K. Inoue-­Nagata1,*, Ramon Jordan2, Jan Kreuze3, Fan Li4, Juan José López-­Moya5, Kristiina Mäkinen6, Kazusato Ohshima7, Stephen J. Wylie8 and ICTV Report Consortium Abstract The family Potyviridae includes plant viruses with single-­stranded, positive-­sense RNA genomes of 8–11 kb and flexuous fila- mentous particles 650–950 nm long and 11–20 nm wide. Genera in the family are distinguished by the host range, genomic features and phylogeny of the member viruses. Most genomes are monopartite, but those of members of the genus Bymovirus are bipartite. Some members cause serious disease epidemics in cultivated plants. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the family Potyviridae, which is available at ictv.global/report/potyviridae. Table 1. Characteristics of members of the family Potyviridae Example potato virus Y-­O (U09509), species Potato virus Y, genus Potyvirus Virion Non-­enveloped, flexuous and filamentous particles, 650–950 nm long and 11–20 nm in diameter with a core capsid protein Genome 8.2–11.5 kb of positive-­sense, single-­stranded, usually monopartite RNA (bipartite in the genus Bymovirus) Replication Cytoplasmic, initiated in virus replication complexes on 6K2-­induced membranous vesicles at endoplasmic reticulum exit sites Translation Directly from genomic RNA Host range Plants; transmission by arthropods, plasmodiophorids (Bymovirus), seeds or pollen Taxonomy Realm Riboviria, kingdom Orthornavirae, phylum Pisuviricota, class Stelpaviricetes, order Patatavirales: >10 genera including >230 species VIRION GENOME The flexuous, filamentous particles are typically 650–950 nm The positive-­sense ssRNA genome ranges from 8.2 kb (members long and 11–20 nm wide, with helical symmetry and a pitch of of the species Artichoke latent virus, genus Macluravirus, and about 3.4–3.5 nm (Fig. 1, Table 1), but members of the genus species Bellflower veinal mottle virus, genus Bevemovirus) to Bymovirus are bipartite with particles of two modal lengths of 11.5 kb (species Celery latent virus, genus Celavirus), with a VPg covalently linked to the 5′-end, and a polyadenylated 3′-terminus 250–300 nm and 500–600 nm. Virions contain a core capsid (Fig. 2). The genome of the celavirus celery latent virus is not protein (CP) of 28.5–47 kDa [1]; the tip of the particle may polyadenylated. Most genomes are monopartite, but those of contain the virus-­encoded proteins genome-­linked protein members of the genus Bymovirus are bipartite. The major large (VPg), helper-­component protease (HC-­Pro), cylindrical ORF of monopartite genomes encodes a polyprotein that is inclusion (CI) and the host factor elF4E. There are serological cleaved into functional proteins at semi-­conserved sites by two relationships among many members. or three viral proteases [2]. Bipartite Bymovirus genomes encode Received 03 February 2022; Accepted 06 February 2022; Published 05 May 2022 Author affiliations: 1Embrapa Vegetables, Brasília, Brazil; 2USDA, Beltsville, MD, USA; 3CIP, Lima, Peru; 4Yunnan Agricultural University, Yunnan, PR China; 5CRAG-­CSIC, Barcelona, Spain; 6University of Helsinki, Helsinki, Finland; 7Saga University, Saga, Japan; 8Murdoch University, Perth, Australia. *Correspondence: Alice K. Inoue-­Nagata, ​alice.​nagata@​embrapa.​br Keywords: ICTV Profile; taxonomy; Potyviridae. Abbreviations: CI, cylindrical inclusion; CP, capsid protein; HC-­Pro, helper-­component protease; VPg, virus protein genome-­linked; VRC, viral replication complex. 001738 © 2022 This is an open-­access article distributed under the terms of the Creative Commons Attribution License. 1 Inoue-­Nagata et al., Journal of General Virology 2022;103:001738 potyviruses and leads to the production of a trans-­frame protein P1N-­PISPO. Some viruses lack one or both of the P1 and HC-­Pro N-­terminal coding regions, and may be replaced by genus-­specific or species-­specific regions. REPLICATION Genomic RNA serves as a template for both translation and replication (reviewed by [4]). The genomic RNA replicates via the production of a full-­length negative-­sense RNA, which takes place in the cytoplasmic viral replication complex (VRC). The VRC is formed by virus proteins, such as NIb, 6K2, VPg, NIa-­Pro, HC-­Pro, CI, and possibly P3 and 6K1, and host factors. The viral genome is transported cell-­to-­cell through the plasmodesmata, probably in the form of particles, involving the coordinated action of CP, CI, P3, 6K2 and P3N-­PIPO [5]. Fig. 1. (Left) Cryo-­electron microscopy reconstruction of a section of a virion of turnip mosaic virus (TuMV). Depicted are the ssRNA (red), and the central globular domain (pale yellow), N-­terminal arm (blue) TAXONOMY and C-­terminal region (grey) of the capsid protein. In the upper section Current taxonomy: ictv.global/taxonomy. Members of different some of the densities are cut-­away. (Right) Cryo-­electron micrograph of genera in the family are distinguished by host range, vector, TuMV virions where the periodic organization of the helical filaments is genomic features and phylogeny, with species demarcation typi- apparent. Bar, ~500 nm. Images are courtesy of R. Cuesta and M. Valle, cally based upon sequence identity of the large ORF (or, if neces- CIC bioGUNE, Spain, based on [7]. sary, the CP-­coding region) being <76% (nt) and <82% (aa) [6]. Thresholds for other coding regions are usually 58% (P1 coding region) or 74–78% (other regions). Members of the family Poty- two polyproteins that are cleaved by two proteases. A second small viridae are transmitted by aphids, eriophyid mites, whiteflies and ORF, PIPO, is generated by a polymerase slippage mechanism and plasmodiophorids, but the vector is not known for members of is expressed as the trans-­frame protein P3N-­PIPO [3]. Another five genera. New species or genera in the family will be considered additional small ORF, PISPO, is generated through a tran- after analyses based on complete genome sequences and addi- scriptional slippage mechanism among sweet potato-­subgroup tional data about biological characteristics. RESOURCES Full ICTV Report on the family Potyviridae: ictv.global/report/​ potyviridae. Funding information Fig. 2. Schematic diagram of the genome organization of potato Production of this summary, the online chapter and associated resources virus Y. VPg, virus protein genome-­linked (indicated by an ellipse at was funded by a grant from the Wellcome Trust (WT108418AIA). the 5′-terminus); P1, protein 1 protease; HC-­Pro, helper component protease; P3, protein 3; PIPO, pretty interesting Potyviridae ORF; 6K1, Acknowledgements Members of the ICTV Report Consortium are Stuart G. Siddell, Elliot 6 kDa peptide 1; CI, cylindrical inclusion; 6K2, 6 kDa peptide 2; NIa-­Pro, J. Lefkowitz, Sead Sabanadzovic, Peter Simmonds, F. Murilo Zerbini, nuclear inclusion a-­protease; NIb, nuclear inclusion b, RNA-­directed Donald B. Smith, and Luisa Rubino. RNA polymerase; CP, capsid protein. Arrowheads indicate cleavage sites of P1 (blue), HC-­Pro (red) and NIa-­Pro (black). Conflicts of interest The authors declare that there are no conflicts of interest. References 4. Mäkinen K, Hafrén A. Intracellular coordination of potyviral RNA func- 1. Martínez-­Turiño S, García JA. Potyviral coat protein and genomic RNA: tions in infection. Front Plant Sci 2014;5:110. A striking partnership leading virion assembly and more. Adv Virus Res 5. Wang A. Cell-­to-­cell movement of plant viruses via plasmodesmata: a 2020;108:165–211. current perspective on potyviruses. Curr Opin Virol 2021;48:10–16. 2. Adams MJ, Antoniw JF, Beaudoin F. Overview and analysis of the 6. Adams MJ, Antoniw JF, Fauquet CM. Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol polyprotein cleavage sites in the family Potyviridae. Mol Plant Pathol 2005;150:459–479. 2005;6:471–487. 7. Cuesta R, Yuste-­Calvo C, Gil-­Cartón D, Sánchez F, Ponz F, et al. 3. Chung BY-­W, Miller WA, Atkins JF, Firth AE. An overlapping essential Structure of Turnip mosaic virus and its viral-­like particles. Sci Rep gene in the Potyviridae. Proc Natl Acad Sci U S A 2008;105:5897–5902. 2019;9:15396. 2