ICTV Report

Subfamily: Betarhabdovirinae

Genus: Cytorhabdovirus

 

Distinguishing features

Historically, two genera of unsegmented plant rhabdoviruses (Cytorhabdovirus and Nucleorhabdovirus) were established based on the sites of member virus replication and morphogenesis. Cytorhabdoviruses are unsegmented plant rhabdoviruses that replicate and mature in the cytoplasm of infected cells. They form a monophyletic group based on well-supported Maximum Likelihood or Maximum Clade Credibility trees inferred from complete L protein sequences. The genus classification based on monophyly has thus far correlated with classification by intracytoplasmic virus maturation.

Virion

Morphology

Enveloped virions are bacilliform, 60–75 nm in diameter and 200–350 nm long (Dietzgen 2002, Jackson et al., 2005a).

Physicochemical and physical properties

The buoyant density in sucrose or potassium tartrate is 1.19–1.20 g cm−3 (Dietzgen 2002). The lipid envelope is derived from the cytoplasmic membranes of plant or insect host cells (Jackson et al., 2005a).

Nucleic acid

The negative-sense, single-stranded RNA genome of 9.8–14.5 kb is unsegmented. Six to eleven mRNAs, one for each of the encoded proteins, have been identified in infected plants.

Proteins

N, P, M, G and L represent the five canonical rhabdovirus structural proteins. P of lettuce necrotic yellows virus (LNYV; species Cytorhabdovirus lactucanecante) and alfalfa dwarf virus (ADV; species Cytorhabdovirus medicagonis) have RNA silencing suppressor activity (Mann et al., 2015, Bejerman et al., 2016, Mann et al., 2016b). The P3 proteins of LNYV and ADV (encoded in the 4b gene) localize to plasmodesmata and trans-complement movement of heterologous viruses between plant cells (Mann et al., 2016a). Colocasia bobone disease-associated virus (CBDaV; species Cytorhabdovirus colocasiae), ADV, strawberry crinkle virus (SCV; species Cytorhabdovirus fragariarugosus), northern cereal mosaic virus (NCMV; species Cytorhabdovirus gramineae) and barley yellow striate mosaic virus (BYSMV; species Cytorhabdovirus hordei) encode small proteins that have the structural characteristics of class 1a viroporins, similar to those detected commonly in mammalian rhabdoviruses. The functions of other accessory proteins are mostly unknown, but it has been recently suggested that P6 of BYSMV acts as a virus effector to downregulate JA signaling and induce plant attractiveness to insects (Gao et al., 2022).

Lipids

The lipoprotein envelope is derived from the host plant or the insect vector (Jackson et al., 2005a). Lipid composition is unknown.

Carbohydrates

LNYV G is glycosylated with a complex network of oligosaccharides containing N-acetylchitobiose, N-linked to asparagine residues. The carbohydrate binds to concanavalin A and can be removed by endoglycosidase F (Dietzgen and Francki 1988).

Genome organisation and replication

The LNYV genome organisation (12.8 kb) is similar to that of Sonchus yellow net virus (SYNV, see genus Betanucleorhabdovirus). Preceded by a non-coding 84 nt leader sequence, the gene order is 3′-N-P-4b-M-G-L-5′ (Figure 1 Cytorhabdovirus). The N gene encodes the nucleoprotein (or nucleocapsid protein), and the P, M, G and L genes encode the phosphoprotein (polymerase cofactor), matrix protein, glycoprotein and RNA polymerase, respectively. The 4b gene encodes a cell-to-cell movement protein (P3). The intergenic regions contain highly conserved consensus sequences. The 5′-non-coding trailer sequence of 187 nt has extensive complementarity to the 3′-leader. The NCMV genome is 13.2 kb with a gene order similar to that of LNYV, except for the presence of three additional small genes of unknown function between the P and M genes, and an additional gene between the G and L genes that encodes a class 1a viroporin-like protein. The genome of BYSMV (12.7 kb) is similar to that of NCMV, except that one of the additional small ORF (P5) located in an alternative frame within the P4 gene and expressed by a leaky scanning mechanism. The genome organisations of lettuce yellow mottle virus (LYMoV; species Cytorhabdovirus lactucamaculante) (12.9 kb), CBDaV (12.2 kb), ADV (14.5 kb) and SCV (14.5 kb) are similar to that of LNYV, except for the presence in SCV and ADV of one additional gene between the G and L genes encoding a class 1a viroporin-like protein. Alternative ORFs within the P gene also occur in several cytorhabdoviruses but it is not known if they are expressed.

Cytorhabdoviruses replicate in the cytoplasm of infected cells in association with masses of thread-like structures (viroplasms) (Jackson et al., 2005a). Virions bud in association with the endoplasmic reticulum (ER) and accumulate in ER-derived vesicles (Chambers et al., 1965, Wolanski and Chambers 1971). A nuclear phase has been suggested but not proven in the replication of some cytorhabdoviruses (e.g., LNYV) (Wolanski and Chambers 1971). Evidence of the nuclear involvement in the replication of others is lacking (e.g., BYSMV). Endogenous transcriptase activity is readily detectable in cytorhabdovirus preparations (Francki and Randles 1972).

Cytorhabdovirus genomes
Figure 1 Cytorhabdovirus. Schematic representation of a selection of cytorhabdovirus genomes shown in reverse (positive-sense) polarity. N, P, M, G and L represent ORFs encoding the structural proteins. ORFs encoding viral cell-to-cell movement proteins (blue) and predicted class 1a viroporin-like proteins (yellow) are shown. Other ORFs encode putative accessory proteins of unknown function, some of which occur as homologous sets (purple, dark green, dark grey or orange). ORFs with no obvious homologues are also shown (grey).­­ In addition to those virus genomes shown: blackcurrant rhabdovirus 2 is similar to lettuce necrotic yellows virus; daphne virus 1 is similar to cabbage cytorhabdovirus 1; Hyptis latent virus is similar to chrysanthemum yellow dwarf virus; Pastinaca cytorhabdovirus 1 is similar to Trifolium pratense virus A; Sambucus virus 1 is similar to Wuhan insect virus 5; strawberry virus 2 is similar to lettuce yellow mottle virus; and Taraxacum cytorhabdovirus 1 is similar to Trifolium pratense virus B.

Biology

A wide variety of monocot and dicot plants are susceptible to cytorhabdoviruses, although each virus usually has a restricted host range. Cytorhabdoviruses are transmitted by aphids (LNYV, ADV), planthoppers (NCMV, BYSMV), leafhoppers (rice stripe mosaic virus (RSMV; species Cytorhabdovirus oryzae) or whiteflies (papaya virus E [PpVE; species Cytorhabdovirus caricae]). Some viruses are also transmitted during vegetative propagation, and some can also be transmitted mechanically from infected sap. Seed transmission has not been reported, but was suggested to be involved in the transmission of Rudbeckia virus 1 (RudV1; species Cytorhabdovirus rudbeckiae) (Lee et al., 2022). In all carefully examined cases, viruses replicate in cells of the insect vector as well as in the plant host (Jackson et al., 2005a, Redinbaugh and Hogenhout 2005).

Species demarcation criteria

Viruses assigned to different species within the genus Cytorhabdovirus have several of the following characteristics: A) their complete genomes have nucleotide sequence identities of less than 75%; B) amino acid sequence identity in all cognate open reading frames is less than 80%; C) they occupy different ecological niches as evidenced by differences in hosts and/or arthropod vectors; and D) they can be clearly distinguished in serological tests or by nucleic acid hybridisation. Cytorhabdovirus species assignments are primarily determined by plant host range and vector specificity. Nucleic acid hybridisation and RT-PCR have been used to provide confirmation of species assignments and serological criteria have enabled verification of common viruses that infect different hosts. However, no cytorhabdovirus species have been defined unambiguously using serology. Hybridisation using cloned probes, RT-PCR and conserved L gene polymerase motif sequences has been used to differentiate viruses within the genus and to identify some strains.

Virus nameAccession numberVirus abbreviation
alfalfa cytorhabdovirus 1OK514706*AlCRV1
alfalfa cytorhabdovirus 2OK514707*AlCRV2
Arctium alphacytorhabdovirus 1BK064262ArcACRV1
Argyranthemum gammacytorhabdovirus 1BK064345ArgGCRV1
Aristolochia associated cytorhabdovirusOR090884AaCV
Artemisia alphacytorhabdovirus 1BK064263ArtACRV1
Artemisia alphacytorhabdovirus 2BK064264ArtACRV2
Artemisia alphacytorhabdovirus 3BK064265ArtACRV3
Artemisia betacytorhabdovirus 1BK064306ArtBCRV1
Baccharis alphacytorhabdovirus 1BK064266BacACRV1
Begonia betacytorhabdovirus 1BK064306BegBCRV1
Betula betacytorhabdovirus 1BK064307BetBCRV1
Betula betacytorhabdovirus 2BK064308BetBCRV2
Bouteloa betacytorhabdovirus 1BK064309BouBCRV1
Cardamine alphacytorhabdovirus 1BK064267CarACRV1
carrot gammacytorhabdovirus 1BK064346CarGCRV1
celery gammacytorhabdovirus 1BK064347CelGCRV1
Chelidonium yellow mottle associated virusOR290114CheYMaV
Chrysanthemum alphacytorhabdovirus 1BK064269ChrACRV1
Chrysanthemum betacytorhabdovirus 1BK064310ChrBCRV1
Cnidium virus 2OQ442952CnV2
Conopholis alphacytorhabdovirus 1BK064270ConACRV1
Coptis gammacytorhabdovirus 1BK064348CopGCRV1
coriander cytorhabdovirus 1OR536958CoCRV1
Corylus betacytorhabdovirus 1BK064311CorBCRV1
Cucubita betacytorhabdovirus 1BK064312CucBCRV1
Cuscuta gammacytorhabdovirus 1BK064349CusGCRV1
Cuscuta gammacytorhabdovirus 2BK064350CusGCRV2
Cynara alphacytorhabdovirus 1BK064271CynACRV1
Cypripedium betacytorhabdovirus 1BK064313CypBCRV1
Cypripedium gammacytorhabdovirus 1BK064351CypGCRV1
Dryobalanops betacytorhabdovirus 1BK064314DryBCRV1
Durio betacytorhabdovirus 1BK064315DurBCRV1
Epipactis gammacytorhabdovirus 1BK064352EpiGCRV1
Euphorbia alphacytorhabdovirus 1BK064272EupACRV1
Ficus alphacytorhabdovirus 1BK064274FicACRV1
Fraxinus gammacytorhabdovirus 1BK064353FraGCRV1
Fraxinus gammacytorhabdovirus 2BJ064354FraGCRV2
garlic alphacytorhabdovirus 1BK064275GarACRV1
Geum alphacytorhabdovirus 1BK064276GeuACRV1
Gleditsia betacytorhabdovirus 1BK064316GleBCRV1
Glycyrrhiza betacytorhabdovirus 1BK064317GlyBCRV1
goji cytorhabdovirus AOR489165GCVA
Hedera alphacytorhabdovirus 1BK064277HedACRV1
Helisoperma gammacytorhabdovirus 1BJ064355HelGCRV1
Hepatica betacytorhabdovirus 1BK064318HepBCRV1
Hibiscus gammacytorhabdovirus 1BK064356HibGCRV1
Howea betacytorhabdovirus 1BK064319HowBCRV1
Ilex alphacytorhabdovirus 1BK064278IleACRV1
Ipomoea betacytorhabdovirus 1BK064320IpoBCRV1
Iranian citrus ringspot-associated virusKP255976*IrCRSaV
ivy vein banding virusGQ249162*; GQ249163*IVBV
Ixeris denticulata associated rhabdovirusOQ927981IdaRV
Justicia betacytorhabdovirus 1BK064321JusBCRV1
Kobresia betacytorhabdovirus 1BK064322KobBCRV1
Leucadendron betacytorhabdovirus 1BK064323LeuBCRV1
Lonas gammacytorhabdovirus 1BK064357LonGCRV1
Lupinus gammacytorhabdovirus 1BK064358LupGCRV1
mango betacytorhabdovirus 1BK064325ManBCRV1
Medicago alphacytorhabdovirus 1BK064279MedACRV1
Mentha alphacytorhabdovirus 1BK064280MenACRV1
Morinda alphacytorhabdovirus 1BK064281MorACRV1
Morus betacytorhabdovirus 1BK064326MorBCRV1
Nitraria betacytorhabdovirus 1BK064327NitBCRV1
oak alphacytorhabdovirus 1BK064283OakACRV1
Ocimum alphacytorhabdovirus 1BK064284OciACRV1
Panicum betacytorhabdovirus 1BK064328PanBCRV1
Passiflora betacytorhabdovirus 1BK064329PasBCRV1
peat soil associated betacytorhabdovirus 1BK064330PSaBCRV1
peat soil associated betacytorhabdovirus 2BK064331PSaBCRV2
Pelargonium alphacytorhabdovirus 1BK064285PelACRV1
Pentaphragma betacytorhabdovirus 1BK064332PenBCRV1
Phellodendron betacytorhabdovirus 1BK064333PheBCRV1
Phyllostachys alphacytorhabdovirus 1BK064286PhyACRV1
Pinellia alphacytorhabdovirus 1BK064287PinACRV1
Plumbago necrotic spot associated virusOR335651PNSaV
Pogostemom alphacytorhabdovirus 1BK064288PogACRV1
Pogostemom alphacytorhabdovirus 2BK064291PogACRV2
Pogostemom alphacytorhabdovirus 3BK064292PogACRV3
Populus betacytorhabdovirus 1BK064334PopBCRV1
Primula alphacytorhabdovirus 1BK064294PriACRV1
Primula alphacytorhabdovirus 2BK064295PriACRV2
Pueraria betacytorhabdovirus 1BK064335PueBCRV1
Rhopalocnemis gammacytorhabdovirus 1BK064359RhoGCRV1
rose alphacytorhabdovirus 1BK064296RosACRV1
Rubus alphacytorhabdovirus 1BK064297RubACRV1
Schiedea betacytorhabdovirus 1BK064338SchBCRV1
Scutellaria alphacytorhabdovirus 1BK064298ScuACRV1
Sesamum betacytorhabdovirus 1BK064336SesBCRV1
Silene gammacytorhabdovirus 1BK064360SilGCRV1
Sophora betacytorhabdovirus 1BK064339SopBCRV1
Tolmiea alphacytorhabdovirus 1BK064299TolACRV1
Trifolium betacytorhabdovirus 1BK064340TriBCRV1
Triticum alphacytorhabdovirus 1BK064300TriACRV1
Utricularia alphacytorhabdovirus 1BK064301UtrACRV1
Vicia betacytorhabdovirus 1BK064341VicBCRV1
wetland metagenome associated alphacytorhabdovirus 1BK064302WMaACRV1
Wurfbainia alphacytorhabdovirus 1BK064303WurACRV1
Zanthoxylum betacytorhabdovirus 1BK064342ZanBCRV1
Zanthoxylum betacytorhabdovirus 2BK064343ZanBCRV2
Zanthoxylum betacytorhabdovirus 3BK064344ZanBCRV3
Zea alphacytorhabdovirus 1BK064304ZeaACRV1

Virus names and virus abbreviations are not official ICTV designations.

* Coding region sequence incomplete