Four principles to establish a universal virus taxonomy.

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes apparent.

Virus taxonomy and the role of the International Committee on Taxonomy of Viruses (ICTV).

The taxonomy of viruses is developed and overseen by the International Committee on Taxonomy of Viruses (ICTV), which scrutinizes, approves and ratifies taxonomic proposals, and maintains a list of virus taxa with approved names (https://ictv.global). The ICTV has approximately 180 members who vote by simple majority. Taxon-specific Study Groups established by the ICTV have a combined membership of over 600 scientists from the wider virology community; they provide comprehensive expertise across the range of known viruses and are major contributors to the creation and evaluation of taxonomic proposals. Proposals can be submitted by anyone and will be considered by the ICTV irrespective of Study Group support. Thus, virus taxonomy is developed from within the virology community and realized by a democratic decision-making process. The ICTV upholds the distinction between a virus or replicating genetic element as a physical entity and the taxon category to which it is assigned. This is reflected by the nomenclature of the virus species taxon, which is now mandated by the ICTV to be in a binomial format (genus + species epithet) and is typographically distinct from the names of viruses. Classification of viruses below the rank of species (such as, genotypes or strains) is not within the remit of the ICTV. This article, authored by the ICTV Executive Committee, explains the principles of virus taxonomy and the organization, function, processes and resources of the ICTV, with the aim of encouraging greater understanding and interaction among the wider virology community.

How To Be a Successful Monopartite Begomovirus in a Bipartite-Dominated World: Emergence and Spread of Tomato Mottle Leaf Curl Virus in Brazil.

Begomoviruses are members of the family Geminiviridae, a large and diverse group of plant viruses characterized by a small circular single-stranded DNA genome encapsidated in twinned quasi-icosahedral virions. Cultivated tomato (Solanum lycopersicum L.) is particularly susceptible and is infected by >100 bipartite and monopartite begomoviruses worldwide. In Brazil, 25 tomato-infecting begomoviruses have been described, most of which are bipartite. Tomato mottle leaf curl virus (ToMoLCV) is one of the most important of these and was first described in the late 1990s but has not been fully characterized. Here, we show that ToMoLCV is a monopartite begomovirus with a genomic DNA similar in size and genome organization to those of DNA-A components of New World (NW) begomoviruses. Tomato plants agroinoculated with the cloned ToMoLCV genomic DNA developed typical tomato mottle leaf curl disease symptoms, thereby fulfilling Koch's postulates and confirming the monopartite nature of the ToMoLCV genome. We further show that ToMoLCV is transmitted by whiteflies, but not mechanically. Phylogenetic analyses placed ToMoLCV in a distinct and strongly supported clade with other begomoviruses from northeastern Brazil, designated the ToMoLCV lineage. Genetic analyses of the complete sequences of 87 ToMoLCV isolates revealed substantial genetic diversity, including five strain groups and seven subpopulations, consistent with a long evolutionary history. Phylogeographic models generated with partial or complete sequences predicted that the ToMoLCV emerged in northeastern Brazil >700 years ago, diversifying locally and then spreading widely in the country. Thus, ToMoLCV emerged well before the introduction of MEAM1 whiteflies, suggesting that the evolution of NW monopartite begomoviruses was facilitated by local whitefly populations and the highly susceptible tomato host. IMPORTANCE Worldwide, diseases of tomato caused by whitefly-transmitted geminiviruses (begomoviruses) cause substantial economic losses and a reliance on insecticides for management. Here, we describe the molecular and biological properties of tomato mottle leaf curl virus (ToMoLCV) from Brazil and establish that it is a NW monopartite begomovirus indigenous to northeastern Brazil. This answered a long-standing question regarding the genome of this virus, and it is part of an emerging group of these viruses in Latin America. This appears to be driven by widespread planting of the highly susceptible tomato and by local and exotic whiteflies. Our extensive phylogenetic studies placed ToMoLCV in a distinct strongly supported clade with other begomoviruses from northeastern Brazil and revealed new insights into the origin of Brazilian begomoviruses. The novel phylogeographic analysis indicated that ToMoLCV has had a long evolutionary history, emerging in northeastern Brazil >700 years ago. Finally, the tools used here (agroinoculation system and ToMoLCV-specific PCR test) and information on the biology of the virus (host range and whitefly transmission) will be useful in developing and implementing integrated pest management (IPM) programs targeting ToMoLCV.

Small but mighty: Functional landscape of the versatile geminivirus-encoded C4 protein.

The fast-paced evolution of viruses enables them to quickly adapt to the organisms they infect by constantly exploring the potential functional landscape of the proteins encoded in their genomes. Geminiviruses, DNA viruses infecting plants and causing devastating crop diseases worldwide, produce a limited number of multifunctional proteins that mediate the manipulation of the cellular environment to the virus' advantage. Among the proteins produced by the members of this family, C4, the smallest one described to date, is emerging as a powerful viral effector with unexpected versatility. C4 is the only geminiviral protein consistently subjected to positive selection and displays a number of dynamic subcellular localizations, interacting partners, and functions, which can vary between viral species. In this review, we aim to summarize our current knowledge on this remarkable viral protein, encompassing the different aspects of its multilayered diversity, and discuss what it can teach us about geminivirus evolution, invasion requirements, and virulence strategies.

Guidance for creating individual and batch latinized binomial virus species names.

The International Committee on Taxonomy of Viruses recently adopted, and is gradually implementing, a binomial naming format for virus species. Although full Latinization of these names remains optional, a standardized nomenclature based on Latinized binomials has the advantage of comparability with all other biological taxonomies. As a language without living native speakers, Latin is more culturally neutral than many contemporary languages, and words built from Latin roots are already widely used in the language of science across the world. Conversion of established species names to Latinized binomials or creation of Latinized binomials de novo may seem daunting, but the rules for name creation are straightforward and can be implemented in a formulaic manner. Here, we describe approaches, strategies and steps for creating Latinized binomials for virus species without prior knowledge of Latin. We also discuss a novel approach to the automated generation of large batches of novel genus and species names. Importantly, conversion to a binomial format does not affect virus names, many of which are created from local languages.

A new bipartite begomovirus naturally infecting Pyrenacantha sp. in Mozambique.

A begomovirus was isolated from a Pyrenacantha sp. plant with yellow mosaic symptoms collected in a maize production field in Mozambique. The complete DNA-A and DNA-B components have a genomic organization typical of Old World, bipartite begomoviruses. Based on the current ICTV species demarcation criteria for the genus Begomovirus, the virus isolate, named Pyrenacantha yellow mosaic virus (PyYMV), is a member of a new species, for which the name "Begomovirus pyrenacanthae" is proposed. Alignment of their common regions (CR) indicated a 35-nt insertion in the DNA-A CR. The nt sequence identity between the CRs is only 83% but increases to 96% when the 35-nt insertion is removed from the alignment. This is the first report of a begomovirus naturally infecting Pyrenacantha spp.

Establishment of five new genera in the family Geminiviridae: Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus.

Geminiviruses are plant-infecting, circular single-stranded DNA viruses that have a geminate virion morphology. These viruses infect both cultivated and non-cultivated monocotyledonous and dicotyledonous plants and have a wide geographical distribution. Nine genera had been established within the family Geminiviridae (Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus, and Turncurtovirus) as of 2020. In the last decade, metagenomics approaches have facilitated the discovery and identification of many novel viruses, among them numerous highly divergent geminiviruses. Here, we report the establishment of five new genera in the family Geminiviridae (Citlodavirus, Maldovirus, Mulcrilevirus, Opunvirus, and Topilevirus) to formally classify twelve new, divergent geminiviruses.

ICTV Virus Taxonomy Profile: Geminiviridae 2021.

The family Geminiviridae includes viruses with mono- or bipartite single-stranded, circular DNA genomes of 2.5-5.2 kb. They cause economically important diseases in most tropical and subtropical regions of the world. Geminiviruses infect dicot and monocot plants and are transmitted by insect vectors. DNA satellites are associated with some geminiviruses. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the family Geminiviridae which is available at ictv.global/report/geminiviridae.

Taxonomy update for the family Alphasatellitidae: new subfamily, genera, and species.

Alphasatellites (family Alphasatellitidae) are circular, single-stranded DNA molecules (~1-1.4 kb) that encode a replication-associated protein and have commonly been associated with some members of the families Geminiviridae, Nanoviridae, and Metaxyviridae (recently established). Here, we provide a taxonomy update for the family Alphasatellitidae following the International Committee on Taxonomy of Viruses (ICTV) Ratification Vote held in March 2021. The taxonomic update includes the establishment of the new subfamily Petromoalphasatellitinae. This new subfamily includes three new genera as well as the genus Babusatellite, which previously belonged to the subfamily Nanoalphasatellitinae. Additionally, three new genera and 14 new species have been established in the subfamily Geminialphasatellitinae, as well as five new species in the subfamily Nanoalphasatellitinae.

Complete genome sequence of a recombinant isolate of yambean mosaic virus from Canavalia ensiformis.

The complete genome sequence of a Brazilian isolate of yambean mosaic virus (YBMV) is presented. High-throughput sequencing (Illumina HiSeq) and Sanger sequencing revealed the complete genome sequence of the YBMV-BRA-6 isolate, found in Canavalia ensiformis. The de novo contigs were assembled into a 9612 nucleotides (nt) long scaffold, excluding the 3'-terminal poly(A) tail, covering the complete genome. The genomic RNA contains an open reading frame (ORF) typical of members of the genus Potyvirus, family Potyviridae, encoding a large putative polyprotein of 3078 amino acids (aa) and a small overlapping PIPO ORF. Pairwise comparisons showed that the YBMV-BRA-6 isolate sequence shares 88.1% nt identity for the complete genome and 90.6% aa identity for the polyprotein with the YBMV-SR isolate. Phylogenetic analysis grouped both isolates together and close to bean common mosaic virus (BCMV). The polyprotein cleavage sites were predicted and a recombination event is described.

First complete genome sequence of an isolate of cowpea severe mosaic virus from South America.

In this study, the complete nucleotide sequence of a Brazilian isolate of cowpea severe mosaic virus (CPSMV) is presented for the first time. To date, the CPSMV-DG isolate, from the USA, is the only one with the complete known genome. High-throughput sequencing (Illumina HiSeq) and Sanger sequencing of the total RNA extract from a cowpea plant collected in Teresina city, Brazil, revealed the genome sequence of the CPSMV-Ter1 isolate. RNA-1 and RNA-2 are, respectively, 5921 and 3465 nucleotides (nt) long without the poly(A) tail, and show 77.91% and 76.08% nt sequence identity with CPSMV-DG, considered the type isolate of the species. The open reading frames (ORFs) were determined and the cleavage sites of the polyproteins were predicted. Although the two isolates show a similar genomic organization, there was a low percentage of sequence identity between Ter1 and DG. Furthermore, pairwise comparisons of a partial RNA-1 fragment between CPSMV-Ter1 and 11 CPSMV isolates from Brazil indicated 94.6 to 94.8% nt and 98.9% to 99.4% aa sequence identities.

Two new begomoviruses infecting tomato and Hibiscus sp. in the Amazon region of Brazil.

Two begomoviruses were isolated in the northern Brazilian state of Pará, infecting non-cultivated Hibiscus sp. and cultivated tomato (Solanum lycopersicum). The complete genomes (DNA-A and DNA-B) of the two viruses showed the typical organization of New World bipartite begomoviruses. Based on the species assignment criteria in the genus Begomovirus, each virus is a member of a new species. The virus from Hibiscus is most closely related to sida yellow mosaic Yucatan virus, while the tomato virus is most closely related to abutilon mosaic Brazil virus and corchorus mottle virus. Recombination events were detected in the DNA-A of the tomato virus, but not in the Hibiscus virus genome. We propose the names "hibiscus golden mosaic virus" (HGMV) and "tomato chlorotic leaf curl virus" (ToCLCV) for the viruses reported in this study.

Evidence for a complex of emergent poleroviruses affecting pepper worldwide.

In recent years, symptoms of vein yellowing and leaf roll in pepper crops associated with the presence of poleroviruses (genus Polerovirus, family Luteoviridae) have been emerging in many countries worldwide. Spain was the first country in Europe where the yellowing disease of pepper was observed. In this work, a polerovirus isolate from Spain that infects pepper and has been shown to be transmitted by the aphid Aphis gossyppii (Spain-Almería 2-2013) was sequenced and compared with isolates from Japan, Israel, China and Australia. The genome (6125 nt in length, GenBank accession number KY523072) of the isolate from Spain has the typical organization of poleroviruses and contains seven open reading frames (ORF0 to ORF5 and ORF3a), putatively encoding proteins P0 to P5 and P3a. A comparison of the sequence from Spain with the four complete sequences available for poleroviruses infecting pepper showed a closer relationship to the isolate from Israel and supports the existence of a complex of at least five polerovirus species. Given that the symptoms caused by all pepper poleroviruses described to date are similar, if not identical, we propose to name them "pepper vein yellows virus 1" to "pepper vein yellows virus 5" (PeVYV-1 to PeVYV-5), with PeVYV-5 corresponding to the polerovirus from Spain described in this work. Our results and those published over the last few years have shown that the emergent poleroviruses threatening pepper crops around the world are highly complex due to recombination events.

Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites.

Nanoviruses and geminiviruses are circular, single stranded DNA viruses that infect many plant species around the world. Nanoviruses and certain geminiviruses that belong to the Begomovirus and Mastrevirus genera are associated with additional circular, single stranded DNA molecules (~ 1-1.4 kb) that encode a replication-associated protein (Rep). These Rep-encoding satellite molecules are commonly referred to as alphasatellites and here we communicate the establishment of the family Alphasatellitidae to which these have been assigned. Within the Alphasatellitidae family two subfamilies, Geminialphasatellitinae and Nanoalphasatellitinae, have been established to respectively accommodate the geminivirus- and nanovirus-associated alphasatellites. Whereas the pairwise nucleotide sequence identity distribution of all the known geminialphasatellites (n = 628) displayed a troughs at ~ 70% and 88% pairwise identity, that of the known nanoalphasatellites (n = 54) had a troughs at ~ 67% and ~ 80% pairwise identity. We use these pairwise identity values as thresholds together with phylogenetic analyses to establish four genera and 43 species of geminialphasatellites and seven genera and 19 species of nanoalphasatellites. Furthermore, a divergent alphasatellite associated with coconut foliar decay disease is assigned to a species but not a subfamily as it likely represents a new alphasatellite subfamily that could be established once other closely related molecules are discovered.

ICTV Virus Taxonomy Profile: Potyviridae.

The Potyviridae is the largest family of RNA plant viruses, members of which have single-stranded, positive-sense RNA genomes and flexuous filamentous particles 680-900 nm long and 11-20 nm wide. There are eight genera, distinguished by the host range, genomic features and phylogeny of the member viruses. Genomes range from 8.2 to 11.3 kb, with an average size of 9.7 kb. 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 taxonomy of the Potyviridae, which is available at www.ictv.global/report/potyviridae.

Genetic variability and population structure of the New World begomovirus Euphorbia yellow mosaic virus.

The emergence of begomoviruses (whitefly-transmitted viruses classified in the genus Begomovirus, family Geminiviridae) in Brazil probably occurred by horizontal transfer from non-cultivated plants after the introduction of Bemisia tabaci MEAM1. The centre of diversity of Euphorbia heterophylla (Euphorbiaceae) is located in Brazil and Paraguay, where it is an invasive species in soybean and other crops. Reports of possible begomovirus infection of E. heterophylla in Brazil date back to the 1950s. In 2011, Euphorbia yellow mosaic virus (EuYMV) was described in symptomatic plants collected in the Brazilian state of Goiás. Here we assess the genetic variability and population structure of begomoviruses infecting E. heterophylla in samples collected throughout nine Brazilian states from 2009 to 2014. A total of 158 and 57 haplotypes were compared in DNA-A and DNA-B datasets, respectively. Analysis comparing population structure in a large sampled area enabled us to differentiate two subpopulations. Further, the application of discriminant analysis of principal components allowed the differentiation of six subpopulations according to sampling locations and in agreement with phylogenetic analysis. In general, negative selection was predominant in all six subpopulations. Interestingly, we were able to reconstruct the phylogeny based on the information from the 23 sites that contributed most to the geographical structure proposed, demonstrating that these polymorphisms hold supporting information to discriminate between subpopulations. These sites were mapped in the genome and compared at the level of amino acid changes, providing insights into how genetic drift and selection contribute to maintain the patterns of begomovirus population variability from a geographical structuring point of view.

ICTV Virus Taxonomy Profile: Geminiviridae.

The geminiviruses are a family of small, non-enveloped viruses with single-stranded, circular DNA genomes of 2500-5200 bases. Geminiviruses are transmitted by various types of insect (whiteflies, leafhoppers, treehoppers and aphids). Members of the genus Begomovirus are transmitted by whiteflies, those in the genera Becurtovirus, Curtovirus, Grablovirus, Mastrevirus and Turncurtovirus are transmitted by specific leafhoppers, the single member of the genus Topocuvirus is transmitted by a treehopper and one member of the genus Capulavirus is transmitted by an aphid. Geminiviruses are plant pathogens causing economically important diseases in most tropical and subtropical regions of the world. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the taxonomy of the Geminiviridae which is available at www.ictv.global/report/geminiviridae.

Two new begomoviruses that infect non-cultivated malvaceae in Brazil.

A high diversity of begomoviruses that infect non-cultivated plants has been noted in Brazil. Here, we report the complete sequences of two new species of bipartite begomoviruses from Sida sp. plants collected in the state of Piauí, northeastern Brazil. The genomes of these viruses show a genomic organization that is typical of New World begomoviruses. In phylogenetic analysis, two closely related viruses (sida angular mosaic virus, SiAMV and sida chlorotic vein virus, SiCVV) clustered with other begomoviruses described in tomato and Sida plants in Brazil. Evidence of recombination is shown among isolates of the species described.