The Ophioviridae is a family of filamentous plant viruses, with single-stranded negative, and possibly ambisense, RNA genomes of 11.3-12.5 kb divided into 3-4 segments, each encapsidated separately. Virions are naked filamentous nucleocapsids, forming kinked circles of at least two different contour lengths. The sole genus, Ophiovirus, includes seven species. Four ophioviruses are soil-transmitted and their natural hosts include trees, shrubs, vegetables and bulbous or corm-forming ornamentals, both monocots and dicots. This is a summary of the International Committee on Taxonomy of Viruses (ICTV) Report on the taxonomy of the Ophioviridae, which is available at http://www.ictv.global/report/ophioviridae.Instituto de Biotecnologia y Biologia MolecularFacultad de Ciencias Agrarias y Forestale

Dal Bó, Elena

Gago-Zachert,  Selma

García, María Laura

Graça, John V.

Hammond, John

ICTV Report Consortium

Moreno, Pedro

Natsuaki, Tomohide

Navarro, José A.

Pallás,Vicente

Reyes, Carina Andrea

Robles Luna, Gabriel

Sasaya, Takahide

Tzanetakis, Ioannis E.

Vaira, Anna María

Verbeek, Martin

Journal of General Virology

SEDICI - Repositorio de la UNLP

ICTV Virus Taxonomy Profile: Ophioviridae
María Laura García,1,* Elena Dal Bó,2 John V. da Graça,3 Selma Gago-Zachert,4 John Hammond,5 Pedro Moreno,6
Tomohide Natsuaki,7 Vicente Pallas,8 Jose A. Navarro,8 Carina A. Reyes,1 Gabriel Robles Luna,1 Takahide Sasaya,9
Ioannis E. Tzanetakis,10 Anna María Vaira,11 Martin Verbeek12 and ICTV Report Consortium
Abstract
The Ophioviridae is a family of filamentous plant viruses, with single-stranded negative, and possibly ambisense, RNA
genomes of 11.3–12.5 kb divided into 3–4 segments, each encapsidated separately. Virions are naked filamentous
nucleocapsids, forming kinked circles of at least two different contour lengths. The sole genus, Ophiovirus, includes seven
species. Four ophioviruses are soil-transmitted and their natural hosts include trees, shrubs, vegetables and bulbous or
corm-forming ornamentals, both monocots and dicots. This is a summary of the International Committee on Taxonomy of
Viruses (ICTV) Report on the taxonomy of the Ophioviridae, which is available at http://www.ictv.global/report/ophioviridae.
VIRION
Particles are non-enveloped, naked filamentous nucleocap-
sids forming either circles (open form) or pseudo-linear
duplex (collapsed form) (Table 1, Fig. 1).
GENOME
The genome of ophioviruses consists of three or four indi-
vidually encapsidated RNA segments (Fig. 2). Members of
the species Citrus psorosis virus [1], Ranunculus white mot-
tle virus, Freesia sneak virus and Blueberry mosaic associated
Table 1. Characteristics of the family Ophioviridae
Typical member: citrus psorosis virus P-121 (RNA1 AY654892; RNA2: AY654893; RNA3: AY654894), species Citrus psorosis virus, genus Ophiovirus
Virion Non-enveloped, nucleocapsids 3 nm in diameter, and 700 nm or 2000 nm long. Pseudo-linear duplex structures are 9–10 nm in diameter
Genome 11.3–12.5 kb of negative-sense, segmented RNA (3 or 4 segments)
Replication Not characterized
Translation From mRNAs, which are complementary to the vRNAs
Host range Citrus, blueberry, pittosporum, lettuce, sowthistle, tulip, ranunculus, anemone, lachenalia and freesia
Taxonomy One genus, Ophiovirus, including seven species
(a) (b)
Fig. 1. Negative contrast electron micrographs (uranyl acetate) of virus
particles. Bar, 100 nm. (a) Open form of the large particle (citrus psoro-
sis virus), and (b) collapsed form (freesia sneak virus) (courtesy of R. G.
Milne).
Received 10 May 2017; Accepted 12 May 2017
Author affiliations: 1Instituto de Biotecnología y Biología Molecular, Universidad de La Plata, La Plata, Argentina; 2Facultad de Ciencias Agrarias y
Forestales, Universidad de La Plata, La Plata, Argentina; 3Texas A and M University-Kingsville, Citrus Center, Weslaco, USA; 4Department of Molecular
Signal Processing, Leibniz Institute of Plant Biochemistry, Halle (Saale), Germany; 5U.S. Department of Agriculture, Agricultural Research Service,
Beltsville, Maryland, USA; 6Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones, Agrarias, Moncada, Valencia, Spain;
7Faculty of Agriculture, Utsunomiya University, Utsunomiya, Japan; 8Instituto de Biología Molecular y Celular de plantas (IBMCP), Universidad
Politecnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain; 9Department of Planning and Coordination, National
Agriculture and Food Research Organization, Tsukuba, Japan; 10Department of Plant Pathology, Division of Agriculture, University of Arkansas, USA; 11
Institute for Sustainable Plant Protection (IPSP) – CNR, Torino, Italy; 12Wageningen Plant Research, Wageningen University and Research, Wageningen,
The Netherlands.
*Correspondence: María Laura García, marialauragarcia2010@gmail.com
Keywords: Ophioviridae; ICTV; taxonomy; citrus psorosis virus; Mirafiori lettuce big-vein virus; lettuce ring necrosis virus; blueberry mosaic
associated virus.
Abbreviations: CP, coat protein; RdRp, RNA-dependent RNA polymerase.
ICTV
ICTV VIRUS TAXONOMY PROFILES
García et al., Journal of General Virology 2017;98:1161–1162
DOI 10.1099/jgv.0.000836
000836
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, distribution and reproduction in any medium, provided the original
author and source are credited.
1161
virus have three RNAs (named RNA1, RNA2 and RNA3)
whereas members of the species Mirafiori lettuce big-vein
virus and Lettuce ring necrosis virus have a fourth RNA
(RNA4) [2]. The genome organization is unknown for
members of the species Tulip mild mottle mosaic virus.
Virions encapsidate both the minus- and positive-sense
RNAs, but a larger amount of RNA of negative polarity is
detected. As virions appear circularized, the presence of pan-
handle structures has been suggested. RNA1 contains two
ORFs in the viral complementary strand (vcRNA) encoding
the 22–25K protein and the RdRp. The 24K protein of citrus
psorosis virus is involved in the misprocessing of miRNA and
RNA silencing suppressor activity. vcRNA2 encodes the cell-
to-cell movement protein (MP), which also has RNA silencing
suppressor activity. Mirafiori lettuce big-vein virus has a sec-
ond putative ORF in vRNA2 that encodes a protein of
unknown function. The coat protein (CP) is encoded by
vcRNA3. A fourth genomic RNA has been reported for Mira-
fiori lettuce big-vein virus and lettuce ring necrosis virus,
encoding putative proteins of unknown function.
TAXONOMY
Ophiovirus is the only genus in the family, including seven
species. CP amino acid sequence alignments show 31–
52% identity between isolates of different species, and 92–
100% identity within a species. The CPs of Mirafiori lettuce
big-vein virus and tulip mild mottle mosaic virus (partial
CDS) share about 80% amino acid sequence identity, thus
warranting an ophiovirus species demarcation criterion
of <85%CP amino acid sequence identity. The RdRp con-
tains the SDD sequence in motif C, a signature for seg-
mented negative-stranded RNA viruses. Phylogenetic
reconstructions using sequences of the conserved core mod-
ule from RdRps of ophioviruses and representative nega-
tive-stranded RNA viruses reinforce their separation as a
monophyletic group. Citrus psorosis virus is present world-
wide, transmitted by vegetative propagation of the host, and
natural dispersion has also been observed. No vector is
known for ranunculus white mottle virus and blueberry
mosaic associated virus. Olpidium virulentus and Olpidium
brassicae fungi transmit Mirafiori lettuce big-vein virus,
tulip mild mottle mosaic virus and lettuce ring necrosis
virus; freesia sneak virus is presumably transmitted by a
member of the genus Olpidium. Ranunculus white mottle
virus has been reported in Italy, France and Germany [3],
and tulip mild mottle mosaic virus in Japan [4]. Mirafiori
lettuce big-vein virus, the causal agent of big-vein disease in
lettuce, probably occurs worldwide. Lettuce ring necrosis
virus is closely associated with lettuce ring necrosis disease
in The Netherlands, Belgium and France [5]. Freesia sneak
virus [6] has been reported in Europe, South Africa, North
America, South Korea and New Zealand. Blueberry mosaic
associated virus is associated with blueberry mosaic disease
found in North and South America, Europe, New Zealand
and Japan [7].
RESOURCE
Full ICTV Online (10th) Report: www.ictv.global/report/
ophioviridae.
Funding information
Production of this summary, the online chapter and associated resour-
ces was funded by a grant from the Wellcome Trust (WT108418AIA).
Acknowledgements
We thank Ulises Mancini (Universidad de La Plata) for helping in the
phylogenetic analysis. Members of the ICTV Report Consortium are
Elliot J. Lefkowitz, Andrew J. Davison, Stuart G. Siddell, Peter Sim-
monds, Michael J. Adams, Donald B. Smith, Richard J. Orton and
Helene Sanfaçon.
Conflicts of interest
The authors declare that there are no conflicts of interest.
References
1. García ML, dal Bó E, Grau O, Milne RG. The closely related citrus
ringspot and citrus psorosis viruses have particles of novel fila-
mentous morphology. J Gen Virol 1994;75:3585–3590.
2. van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JF.
Nucleotide sequence and genomic organization of an ophiovirus
associated with lettuce big-vein disease. J Gen Virol 2002;83:2869–
2877.
3. Vaira AM, Accotto GP, Costantini A, Milne RG. The partial sequence
of RNA 1 of the ophiovirus Ranunculus white mottle virus indicates
its relationship to rhabdoviruses and provides candidate primers
for an ophiovirus-specific RT-PCR test. Arch Virol 2003;148:1037–
1050.
4. Morikawa T, Nomura Y, Yamamoto T, Natsuaki T. Partial character-
ization of virus-like particles associated with tulip mild mottle
mosaic. Jap J Phytopathol 1995;61:578–581.
5. Torok VA, Vetten HJ. Identification and molecular characterisation
of a new ophiovirus associated with lettuce ring necrosis disease.
Proceedings of Arbeitskreis Viruskrankheiten der Pflanzen.
Heidelberg, Germany; 2003.
6. Vaira AM, Lisa V, Costantini A, Masenga V, Rapetti S et al. Ophioviruses
infecting ornamentals and a probable new species associated with a
severe disease in freesia.Acta Hortic 2006;722:191–200.
7. Thekke-Veetil T, Ho T, Keller KE, Martin RR, Tzanetakis IE. A new
ophiovirus is associated with blueberry mosaic disease. Virus Res
2014;189:92–96.
RNA1
~8 kb
v5′ 3′
260–280K RdRp
vc3′ 5′
22–25K
v5′ 3′
10K
RNA2
~1.8 kb
v5′ 3′ v5′ 3′RNA3
~1.5 kb
RNA4
~1.4 kbvc3′ 5′
MP
vc3′ 5′
CP
vc3′ 5′
37K
10.6K
Fig. 2. Genome organization of the genus Ophiovirus. Mirafiori lettuce
big-vein virus is shown (modified from [2]). Boxes represent ORFs. The
length of the RNA segments and the predicted sizes of the ORF prod-
ucts are indicated. RNA4 is not reported for all ophioviruses. v, viral
RNA; vc, viral complementary RNA; RdRp, RNA polymerase; MP, move-
ment protein; CP, coat protein.
García et al., Journal of General Virology 2017;98:1161–1162
1162


English

ICTV virus taxonomy profile: Ophioviridae

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ICTV Virus Taxonomy Profile: OphioviridaeMaría Laura García,1,* Elena Dal Bó,2 John V. da Graça,3 Selma Gago-Zachert,4 John Hammond,5 Pedro Moreno,6Tomohide Natsuaki,7 Vicente Pallas,8 Jose A. Navarro,8 Carina A. Reyes,1 Gabriel Robles Luna,1 Takahide Sasaya,9Ioannis E. Tzanetakis,10 Anna María Vaira,11 Martin Verbeek12 and ICTV Report ConsortiumAbstractThe Ophioviridae is a family of filamentous plant viruses, with single-stranded negative, and possibly ambisense, RNAgenomes of 11.3–12.5 kb divided into 3–4 segments, each encapsidated separately. Virions are naked filamentousnucleocapsids, forming kinked circles of at least two different contour lengths. The sole genus, Ophiovirus, includes sevenspecies. Four ophioviruses are soil-transmitted and their natural hosts include trees, shrubs, vegetables and bulbous orcorm-forming ornamentals, both monocots and dicots. This is a summary of the International Committee on Taxonomy ofViruses (ICTV) Report on the taxonomy of the Ophioviridae, which is available at http://www.ictv.global/report/ophioviridae.VIRIONParticles are non-enveloped, naked filamentous nucleocap-sids forming either circles (open form) or pseudo-linearduplex (collapsed form) (Table 1, Fig. 1).GENOMEThe genome of ophioviruses consists of three or four indi-vidually encapsidated RNA segments (Fig. 2). Members ofthe species Citrus psorosis virus [1], Ranunculus white mot-tle virus, Freesia sneak virus and Blueberry mosaic associatedTable 1. Characteristics of the family OphioviridaeTypical member: citrus psorosis virus P-121 (RNA1 AY654892; RNA2: AY654893; RNA3: AY654894), species Citrus psorosis virus, genus OphiovirusVirion Non-enveloped, nucleocapsids 3 nm in diameter, and 700 nm or 2000 nm long. Pseudo-linear duplex structures are 9–10 nm in diameterGenome 11.3–12.5 kb of negative-sense, segmented RNA (3 or 4 segments)Replication Not characterizedTranslation From mRNAs, which are complementary to the vRNAsHost range Citrus, blueberry, pittosporum, lettuce, sowthistle, tulip, ranunculus, anemone, lachenalia and freesiaTaxonomy One genus, Ophiovirus, including seven species(a) (b)Fig. 1. Negative contrast electron micrographs (uranyl acetate) of virusparticles. Bar, 100 nm. (a) Open form of the large particle (citrus psoro-sis virus), and (b) collapsed form (freesia sneak virus) (courtesy of R. G.Milne).Received 10 May 2017; Accepted 12 May 2017Author affiliations: 1Instituto de Biotecnología y Biología Molecular, Universidad de La Plata, La Plata, Argentina; 2Facultad de Ciencias Agrarias yForestales, Universidad de La Plata, La Plata, Argentina; 3Texas A and M University-Kingsville, Citrus Center, Weslaco, USA; 4Department of MolecularSignal Processing, Leibniz Institute of Plant Biochemistry, Halle (Saale), Germany; 5U.S. Department of Agriculture, Agricultural Research Service,Beltsville, Maryland, USA; 6Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones, Agrarias, Moncada, Valencia, Spain;7Faculty of Agriculture, Utsunomiya University, Utsunomiya, Japan; 8Instituto de Biología Molecular y Celular de plantas (IBMCP), UniversidadPolitecnica de Valencia-Consejo Superior de Investigaciones Científicas, Valencia, Spain; 9Department of Planning and Coordination, NationalAgriculture and Food Research Organization, Tsukuba, Japan; 10Department of Plant Pathology, Division of Agriculture, University of Arkansas, USA; 11Institute for Sustainable Plant Protection (IPSP) – CNR, Torino, Italy; 12Wageningen Plant Research, Wageningen University and Research, Wageningen,The Netherlands.*Correspondence: María Laura García, marialauragarcia2010@gmail.comKeywords: Ophioviridae; ICTV; taxonomy; citrus psorosis virus; Mirafiori lettuce big-vein virus; lettuce ring necrosis virus; blueberry mosaicassociated virus.Abbreviations: CP, coat protein; RdRp, RNA-dependent RNA polymerase.ICTVICTV VIRUS TAXONOMY PROFILESGarcía et al., Journal of General Virology 2017;98:1161–1162DOI 10.1099/jgv.0.000836000836This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, distribution and reproduction in any medium, provided the originalauthor and source are credited.1161virus have three RNAs (named RNA1, RNA2 and RNA3)whereas members of the species Mirafiori lettuce big-veinvirus and Lettuce ring necrosis virus have a fourth RNA(RNA4) [2]. The genome organization is unknown formembers of the species Tulip mild mottle mosaic virus.Virions encapsidate both the minus- and positive-senseRNAs, but a larger amount of RNA of negative polarity isdetected. As virions appear circularized, the presence of pan-handle structures has been suggested. RNA1 contains twoORFs in the viral complementary strand (vcRNA) encodingthe 22–25K protein and the RdRp. The 24K protein of citruspsorosis virus is involved in the misprocessing of miRNA andRNA silencing suppressor activity. vcRNA2 encodes the cell-to-cell movement protein (MP), which also has RNA silencingsuppressor activity. Mirafiori lettuce big-vein virus has a sec-ond putative ORF in vRNA2 that encodes a protein ofunknown function. The coat protein (CP) is encoded byvcRNA3. A fourth genomic RNA has been reported for Mira-fiori lettuce big-vein virus and lettuce ring necrosis virus,encoding putative proteins of unknown function.TAXONOMYOphiovirus is the only genus in the family, including sevenspecies. CP amino acid sequence alignments show 31–52% identity between isolates of different species, and 92–100% identity within a species. The CPs of Mirafiori lettucebig-vein virus and tulip mild mottle mosaic virus (partialCDS) share about 80% amino acid sequence identity, thuswarranting an ophiovirus species demarcation criterionof <85%CP amino acid sequence identity. The RdRp con-tains the SDD sequence in motif C, a signature for seg-mented negative-stranded RNA viruses. Phylogeneticreconstructions using sequences of the conserved core mod-ule from RdRps of ophioviruses and representative nega-tive-stranded RNA viruses reinforce their separation as amonophyletic group. Citrus psorosis virus is present world-wide, transmitted by vegetative propagation of the host, andnatural dispersion has also been observed. No vector isknown for ranunculus white mottle virus and blueberrymosaic associated virus. Olpidium virulentus and Olpidiumbrassicae fungi transmit Mirafiori lettuce big-vein virus,tulip mild mottle mosaic virus and lettuce ring necrosisvirus; freesia sneak virus is presumably transmitted by amember of the genus Olpidium. Ranunculus white mottlevirus has been reported in Italy, France and Germany [3],and tulip mild mottle mosaic virus in Japan [4]. Mirafiorilettuce big-vein virus, the causal agent of big-vein disease inlettuce, probably occurs worldwide. Lettuce ring necrosisvirus is closely associated with lettuce ring necrosis diseasein The Netherlands, Belgium and France [5]. Freesia sneakvirus [6] has been reported in Europe, South Africa, NorthAmerica, South Korea and New Zealand. Blueberry mosaicassociated virus is associated with blueberry mosaic diseasefound in North and South America, Europe, New Zealandand Japan [7].RESOURCEFull ICTV Online (10th) Report: www.ictv.global/report/ophioviridae.Funding informationProduction of this summary, the online chapter and associated resour-ces was funded by a grant from the Wellcome Trust (WT108418AIA).AcknowledgementsWe thank Ulises Mancini (Universidad de La Plata) for helping in thephylogenetic analysis. Members of the ICTV Report Consortium areElliot J. Lefkowitz, Andrew J. Davison, Stuart G. Siddell, Peter Sim-monds, Michael J. Adams, Donald B. Smith, Richard J. Orton andHelene Sanfaçon.Conflicts of interestThe authors declare that there are no conflicts of interest.References1. García ML, dal Bó E, Grau O, Milne RG. The closely related citrusringspot and citrus psorosis viruses have particles of novel fila-mentous morphology. J Gen Virol 1994;75:3585–3590.2. van der Wilk F, Dullemans AM, Verbeek M, van den Heuvel JF.Nucleotide sequence and genomic organization of an ophiovirusassociated with lettuce big-vein disease. J Gen Virol 2002;83:2869–2877.3. Vaira AM, Accotto GP, Costantini A, Milne RG. The partial sequenceof RNA 1 of the ophiovirus Ranunculus white mottle virus indicatesits relationship to rhabdoviruses and provides candidate primersfor an ophiovirus-specific RT-PCR test. Arch Virol 2003;148:1037–1050.4. Morikawa T, Nomura Y, Yamamoto T, Natsuaki T. Partial character-ization of virus-like particles associated with tulip mild mottlemosaic. Jap J Phytopathol 1995;61:578–581.5. Torok VA, Vetten HJ. Identification and molecular characterisationof a new ophiovirus associated with lettuce ring necrosis disease.Proceedings of Arbeitskreis Viruskrankheiten der Pflanzen.Heidelberg, Germany; 2003.6. Vaira AM, Lisa V, Costantini A, Masenga V, Rapetti S et al. Ophiovirusesinfecting ornamentals and a probable new species associated with asevere disease in freesia.Acta Hortic 2006;722:191–200.7. Thekke-Veetil T, Ho T, Keller KE, Martin RR, Tzanetakis IE. A newophiovirus is associated with blueberry mosaic disease. Virus Res2014;189:92–96.RNA1~8 kbv5′ 3′260–280K RdRpvc3′ 5′22–25Kv5′ 3′10KRNA2~1.8 kbv5′ 3′ v5′ 3′RNA3~1.5 kbRNA4~1.4 kbvc3′ 5′MPvc3′ 5′CPvc3′ 5′37K10.6KFig. 2. Genome organization of the genus Ophiovirus. Mirafiori lettucebig-vein virus is shown (modified from [2]). Boxes represent ORFs. Thelength of the RNA segments and the predicted sizes of the ORF prod-ucts are indicated. RNA4 is not reported for all ophioviruses. v, viralRNA; vc, viral complementary RNA; RdRp, RNA polymerase; MP, move-ment protein; CP, coat protein.García et al., Journal of General Virology 2017;98:1161–11621162

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ICTV virus taxonomy profile: Ophioviridae

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