Satellites and Other Virus-dependent Nucleic Acids

Chapter Version: ICTV Ninth Report; 2009 Taxonomy Release


Satellites are subviral agents which lack genes that could encode functions needed for replication. Thus for their multiplication they depend on the co-infection of a host cell with a helper virus. Satellite genomes have a substantial portion or all of their nucleotide sequences distinct from those of the genomes of their helper virus.

According to this definition, two major classes of satellites may be distinguished. Satellite viruses encode a structural protein that encapsidates their genome and so have nucleoprotein components distinct from those of their helper viruses. Satellite nucleic acids encode either non-structural proteins, or no proteins at all, and are encapsidated by the CP of helper viruses.

In addition to the true satellites, this chapter also describes subviral agents (nucleic acids) that depend upon viruses in a variety of ways. Satellite-like nucleic acids resemble satellites because they do not encode a replicase but differ because they encode a function necessary for the biological success of the associated virus. They can therefore be considered as components that remedy a deficiency in a defective virus. They have sometimes been classified as part of the genome of the virus they assist but they can also be dispensable because they are not always found in association with their helper virus. Examples include RNAs associated with groundnut rosette virus (genus Umbravirus) or with beet necrotic yellow vein virus (genus Benyvirus), that contribute to vector transmissibility and DNAs associated with begomoviruses (betasatellites) that encode a pathogenicity determinant.

A final group of agents described are nucleic acids capable of autonomous replication and which therefore are not strictly satellites although the term has sometimes been loosely applied to them. These agents are dependent on their helper viruses for various functions such as encapsidation, cell-to-cell and long-distance movement and vector transmission. Examples are the alphasatellites (DNAs that encode a replication initiator protein) or the RNAs associated with some poleroviruses that appear to encode a carmovirus-like RdRp.

The distinction between satellite nucleic acids, satellite-like nucleic acids and virus genomic components can be subtle and these agents are not always easy to categorize.

Distinguishing features

Satellites are genetically distinct from their helper virus with a nucleotide sequence that is substantially different from that of their helper virus. However, the genomes of most satellites have short sequences, often at the termini, that are identical to the genome of the helper virus. This is presumably linked to the dependence of nucleic acids of both satellite and helper virus on the same viral polymerase and host-encoded proteins for replication. Satellites are distinct from defective interfering (DI) RNAs or defective RNAs because such RNAs are derived from their “helper” virus genomes. Nevertheless, satellite viruses may form their own DI RNAs that specifically interfere with the satellite virus genomic RNA, as has been shown for satellite panicum mosaic virus. Recombination can occur between satellites and their helper viruses. For example, chimeric molecules can be formed from a satellite RNA associated with turnip crinkle virus (genus Carmovirus) and parts of the helper virus genome.

Satellites do not constitute a homogeneous taxonomic group and are not formally classified into species and higher taxa by ICTV. The descriptions in this section are meant only to provide a classification framework and a nomenclature to assist in the description and identification of satellites and other virus-dependent nucleic acids. The arrangement adopted is based largely on features of the genetic material of the satellites. The physicochemical and biological features of the helper virus and of the helper virus host are important secondary characters.

There appears to be no taxonomic correlation between the viruses that are associated with satellites. Satellites would appear to have arisen independently a number of times during virus evolution. A further complication is that some viruses are associated with more than one satellite and some satellites are supported by more than one species of helper virus. Satellites can even depend on both a second satellite and a helper virus for multiplication.

The first satellites characterized were mostly ssRNA satellites that use ssRNA plant viruses as helpers. It can be very difficult to distinguish between satellite RNA and viral genomic RNA (e. g., dsRNA satellites of fungus viruses) and it is very likely that other satellites, some with novel combinations of characters, remain to be discovered.

Categories of satellites

Satellite viruses:

  1. Chronic bee-paralysis virus-associated satellite virus
  2. Satellites that resemble tobacco necrosis satellite virus
  3. Nodavirus-associated satellite virus
  4. Adenovirus-associated satellite virus (Dependovirus)
  5. Mimivirus-associated satellite virus (Sputnik, virophage)

Virus-dependent nucleic acids:

  1. Single stranded DNAs

6a    Alphasatellites (encoding a replication initiator protein)

6b   Betasatellites (encoding a pathogenicity determinant)

  1. Double stranded RNAs
  2. Single stranded RNAs

8a    Large linear single stranded satellite RNAs

8b   Small linear single stranded satellite and satellite-like RNAs

8c    Small circular single stranded satellite RNAs

8d   Hepadnavirus-associated satellite-like RNAs (Deltavirus)

8e    Polerovirus-associated RNAs

Satellite Viruses

These satellites encode a structural protein to encapsidate their genomes. The satellite virus particles are antigenically, and usually morphologically, distinct from those of the helper virus. Five subgroups of satellite viruses are currently distinguished.

1 Chronic bee-paralysis associated satellite virus

Satellite virus particles are found in bees infected with the helper, chronic bee-paralysis virus (CBPV; a virus not yet classified). Particles are about 12 nm in diameter and serologically unrelated to those of CBPV. The satellite interferes with CBPV replication.

List of group members


Chronic bee-paralysis satellite virus




2 Satellites that resemble tobacco necrosis satellite virus

These satellite virus particles are found in plant hosts in association with taxonomically diverse helper viruses. The T=1 isometric particles are about 17 nm in diameter. The capsid consists of 60 copies of a single protein of 17–24 kDa, which is encoded by the satellite virus genome (positive sense ssRNA). The genomes of some satellite viruses contain a second ORF.

List of group members


Satellite viruses associated with viruses in the familyTombusviridae

 Maize white line mosaic satellite virus



 Panicum mosaic satellite virus



 Tobacco necrosis satellite virus



Satellite viruses associated with viruses in the familyVirgaviridae

 Tobacco mosaic satellite virus




3 Nodavirus-associated satellite virus

Satellite virus particles are found in Macrobrachium rosenbergii (giant river prawn) infected with Macrobrachium rosenbergii nodavirus (MrNV; a virus not yet classified but clearly related to viruses in the family Nodaviridae). The XSV (extra small virus) satellite virus particles are about 15 nm in diameter and serologically unrelated to those of MrNV. XSV is a positive-sense single-stranded RNA, about 800 bases in size, encoding a 17 kDa capsid protein. The mixed infection of MrNV and XSV is implicated in white spot disease of prawns.

List of group members


Macrobrachium rosenbergii nodavirus XSV (extra small virus)




4 Adenovirus-associated satellite virus (Dependovirus)

Adenovirus-associated (AAV) satellite virus particles are found in humans, domesticated animals, fowl and in tissue or cell cultures as co-infections with a helper virus. The single stranded 5 kb DNA genome encodes three structural proteins (VP1, −2 and −3). The 26 nm T=1 particles have a 10:1:1 ratio of VP3:VP2:VP1. Smaller particles about 12 nm in diameter only contain the 60 kDa VP3 protein. AAV satellite viruses are dependent on adenoviruses (or herpesviruses) for replication and cap functions. This group of satellites is anomalous, having been placed in a genus Dependovirus within the family Parvoviridae, although they meet all definitions for an authentic satellite virus. For more details see the section on genus Dependovirus.

List of group members

See tables for the genus Dependovirus in the Parvoviridae chapter.

5 Mimivirus-associated satellite virus (Sputnik, virophage)

Acanthamoeba polyphaga mimivirus (genus Mimivirus) is an extremely large (ca. 1.2 Mbp) virus with a dsDNA genome that infects amoebae of the genus Acanthamoeba. A mimivirus strain (sometimes called mamavirus) isolated from A. castellanii supports a 50 nm T=27 satellite virus, referred to as Sputnik (=satellite in Russian). The satellite virus has a circular dsDNA genome of 18 kbp that is predicted to code for about 22 proteins. Sputnik does not replicate in either host in the absence of the helper virus.

List of group members


Acanthamoeba castellanii mamavirus-associated satellite virus (Sputnik)


(Sputnik; virophage)


Virus-dependent Nucleic Acids

This category includes a diverse range of DNA and RNA molecules that do not encode a capsid protein but are packaged in capsids encoded by their helper virus. Those that encode a function necessary for the biological success of the associated virus are described as “satellite-like”.

6 Single stranded DNAs

6a Alphasatellites

These molecules are not strictly satellites because they encode a rolling-circle replication initiator protein (known as the replication-associated protein [Rep]) with similarity to the master Rep encoding genomic components (DNA-R) of nanoviruses. They are capable of autonomous replication in host cells, have a stem-loop region containing the ubiquitous nonanucleotide TAA/GTATTAC, and depend on their helper viruses for encapsidation, movement in plants and insect transmission. Some are associated with viruses in the genus Begomovirus and are typically about 1.4 kb, half the size of their helper viruses. Others are associated with multipartite genome viruses of the family Nanoviridae and are approximately the same size (ca. 1 kb) as the genomic components of their helper viruses (but are not derived from them). The presence of alphasatellites in begomovirus and nanovirid infections may reduce symptom severity, suggesting interference akin to that seen with defective interfering DNAs. Recent results have shown that the Rep encoded by at least some alphasatellites associated with begomoviruses suppresses host defenses based on RNA interference.

List of group members


Begomovirus-associated alphasatellites

 Ageratum yellow vein alphasatellite



 Ageratum yellow vein India alphasatellite



 Ageratum yellow vein Kenya alphasatellite



 Ageratum yellow vein Pakistan alphasatellite



 Ageratum yellow vein Singapore alphasatellite



 Cotton leaf curl Dabwali alphasatellite



 Cotton leaf curl Gezira alphasatellite



 Cotton leaf curl Multan alphasatellite



 Cotton leaf curl Shadadpur alphasatellite



 Duranta leaf curl alphasatellite



 Gossypium darwinii symptomless alphasatellite



 Gossypium davidsonii symptomless alphasatellite



 Gossypium mustilinum symptomless alphasatellite



 Hibiscus leaf curl alphasatellite



 Malvastrum yellow mosaic alphasatellite



 Malvastrum yellow mosaic Hainan alphasatellite



 Okra leaf curl alphasatellite



 Okra leaf curl Barombi alphasatellite



 Okra leaf curl Burkina Faso alphasatellite



 Okra leaf curl Mali alphasatellite



 Sida yellow vein Vietnam alphasatellite



 Tobacco curly shoot alphasatellite



 Tomato leaf curl Pakistan alphasatellite



 Tomato yellow leaf curl China alphasatellite



Babu- and nanovirus-associated alphasatellites

 Banana bunchy top S1 alphasatellite



 Banana bunchy top S2 alphasatellite



 Banana bunchy top S3 alphasatellite



 Banana bunchy top W1 alphasatellite



 Banana bunchy top Y alphasatellite



 Faba bean necrotic yellows C1 alphasatellite



 Faba bean necrotic yellows C11 alphasatellite



 Faba bean necrotic yellows C7 alphasatellite



 Faba bean necrotic yellows C9 alphasatellite



 Milk vetch dwarf C1 alphasatellite



 Milk vetch dwarf C10 alphasatellite



 Milk vetch dwarf C2 alphasatellite



 Milk vetch dwarf C3 alphasatellite



 Subterranean clover stunt C2 alphasatellite



 Subterranean clover stunt C6 alphasatellite



Possible member



 Coconut foliar decay alphasatellite




6b Betasatellites

These are satellite-like circular ssDNA components, usually about 1.3 kb in size that are associated with viruses in the genus Begomovirus. Although initially identified only in association with monopartite begomoviruses, recently they have been increasingly identified in association with bipartite begomoviruses. All betasatellites have a stem-loop region containing the ubiquitous nonanucleotide TAATATTAC and an associated highly conserved sequence located immediately upstream (the function of which remains uncertain), a conserved ORF (termed βC1; encoding a protein that is a pathogenicity determinant and a suppressor of host defenses based on RNA interference), and an A-rich region that may reflect size adaptation for maintenance of the component by the helper begomovirus. The betasatellite DNAs readily recombine with the helper begomovirus genome and such recombinants may retain a biological activity similar to the parental betasatellite. Pairwise comparisons between sequences have shown that a sequence identity of about 78% is an appropriate demarcation threshold for distinguishing between betasatellites.

List of group members


Ageratum leaf curl Cameroon betasatellite



Ageratum yellow leaf curl betasatellite



Ageratum yellow vein betasatellite



Ageratum yellow vein Sri Lanka betasatellite



Alternanthera yellow vein betasatellite



Bean leaf curl China betasatellite



Bhendi yellow vein betasatellite



Cardiospemum yellow leaf curl betasatellite



Chilli leaf curl betasatellite



Cotton leaf curl Gezira betasatellite



Cotton leaf curl Multan betasatellite



Croton yellow vein mosaic betasatellite



Emilia yellow vein betasatellite



Erectites yellow mosaic betasatellite



Eupatorium yellow vein betasatellite



Honeysuckle yellow vein betasatellite



Honeysuckle yellow vein Japan betasatellite



Honeysuckle yellow vein Kochi betasatellite



Honeysuckle yellow vein mosaic betasatellite



Honeysuckle yellow vein mosaic Hyogo betasatellite



Honeysuckle yellow vein mosaic Nara betasatellite



Kenaf leaf curl betasatellite



Leucas zeylanica yellow vein betasatellite



Lindernia anagallis yellow vein betasatellite



Ludwigia yellow vein betasatellite



Luffa leaf distortion betasatellite



Malvastrum leaf curl betasatellite



Malvastrum yellow vein betasatellite



Malvastrum yellow vein Yunnan betasatellite



Mesta yellow vein mosaic betasatellite



Okra leaf curl betasatellite



Papaya leaf curl betasatellite



Radish leaf curl betasatellite



Sida leaf curl betasatellite



Sida yellow mosaic China betasatellite



Sida yellow vein betasatellite



Sida yellow vein mosaic betasatellite



Sida yellow vein Vietnam betasatellite



Siegesbeckia yellow vein betasatellite



Siegesbeckia yellow vein Guangxi betasatellite



Tobacco curly shoot betasatellite



Tobacco leaf curl betasatellite



Tomato leaf curl Bangalore betasatellite



Tomato leaf curl Bangladesh betasatellite



Tomato leaf curl betasatellite



Tomato leaf curl China betasatellite



Tomato leaf curl Java betasatellite



Tomato leaf curl Joydebpur betasatellite



Tomato leaf curl Karnataka betasatellite



Tomato leaf curl Laos betasatellite



Tomato leaf curl Maharastra betasatellite



Tomato leaf curl Patna betasatellite



Tomato leaf curl Philippines betasatellite



Tomato leaf curl virus satellite



Tomato yellow dwarf betasatellite



Tomato yellow leaf curl China betasatellite



Tomato yellow leaf curl Thailand betasatellite



Tomato yellow leaf curl Vietnam betasatellite



Tomato yellow leaf curl Yunnan betasatellite



Vernonia yellow vein betasatellite



Zinnia leaf curl betasatellite




7 Double stranded RNAs

Most satellites in this category are found in association with viruses in the families Totiviridae and Partitiviridae. The dsRNAs range in size from 0.5 to 1.8 kbp and are encapsidated using the helper virus capsid protein. These particles often also contain a positive sense single stranded copy of the dsRNA. The satellite dsRNAs associated with helper viruses in the genus Totivirus encode a secreted preprotoxin that is lethal to sensitive cells (virus-free or containing helper virus only). The presence of satellites in helper totivirus cultures imparts self-protection against the secreted toxin and confers ecological advantage by killing competing virus- or satellite-free fungi. The satellite dsRNAs associated with partitiviruses do not code for functional proteins and their biological significance is not known.

List of group members


Satellites associated with viruses in the familyTotiviridae

 M satellites of Saccharomyces cerevisiae L-A virus










 M satellites of Ustilago maydis virus H












 Satellites of Trichomonas vaginalis T1 virus



Possible member



 M satellite of Zygosaccharomyces balii virus



Satellites associated with viruses in the familyPartitiviridae

 Satellite of Atkinsonella hypoxylon virus



 Satellites of Discula destructiva virus 1



 dsRNA 3






 Satellite of Gremmeniella abietina virus MS1



 Satellite of Penicillium stoloniferum virus F



Possible members



 Satellites of Amasya cherry disease-associated virus

 Satellite A



 Satellite B



 Satellites of cherry chlorotic rusty spot -associated virus

 Satellite A



 Satellite B



 Satellite C



Satellites associated with viruses in the familyReoviridae

 Bombyx mori cypovirus 1 satellite RNA



* Abbreviations: Sat, satellite; Seg, segment.

8 Single stranded RNAs

8a Large linear single stranded satellite RNAs

This category comprises satellites with genomes that are 0.8 to 1.5 kb in size and encode a non-structural protein that, at least in some cases, is essential for satellite RNA multiplication. Little sequence homology exists between the satellites and their helpers, some satellites can be exchanged among different helper viruses. These satellites rarely modify the disease induced in host plants by the helper virus. Most are associated with helper viruses in the family Secoviridae.

List of group members


Satellite RNAs associated with viruses in the familySecoviridae


 Arabis mosaic virus large satellite RNA


 Beet ringspot virus satellite RNA (TBRV-S serotype satellite RNA)


 Blackcurrant reversion virus satellite RNA


 Chicory yellow mottle virus large satellite RNA


 Grapevine Bulgarian latent virus satellite RNA


 Grapevine fanleaf virus satellite RNA


 Myrobalan latent ringspot virus satellite RNA


 Strawberry latent ringspot virus satellite RNA


 Tomato black ring virus satellite RNA (TBRV-G serotype satellite RNA)


Satellite RNAs associated with viruses in the familyAlphaflexiviridae


 Bamboo mosaic virus satellite RNA


Possible member


 Beet necrotic yellow vein virus RNA5*


* Non-essential genome component that may be regarded as a satellite-like RNA. Beet necrotic yellow vein virus is a member of the genus Benyvirus.

8b Small linear single stranded satellite and satellite-like RNAs

These satellites have a strictly linear genome of less than 0.7 kb that does not encode functional proteins. Some satellites can attenuate the symptoms induced by helper virus infection, whereas other satellites can exacerbate the symptoms.

List of group members


Satellite RNAs associated with viruses in the familyTombusviridae

 Artichoke mottled crinkle virus satellite RNA


 Black beet scorch virus satellite RNA


 Carnation Italian ringspot virus satellite RNA


 Cymbidium ringspot virus satellite RNA


 Panicum mosaic virus satellite RNA


 Pelargonium leaf curl virus satellite RNA


 Petunia asteroid mosaic virus satellite RNA


 Tobacco necrosis virus small satellite RNA


 Tomato bushy stunt virus satellite RNA (several types)


Satellite RNAs associated with viruses in the familyBromoviridae

 Cucumber mosaic virus satellite RNA (several types)


 Peanut stunt virus satellite RNA


Satellite RNAs associated with viruses in the genus Umbravirus

 Carrot mottle mimic virus satellite RNA


 Groundnut rosette virus satellite RNA*


 Pea enation mosaic virus satellite RNA


 Tobacco bushy top virus satellite RNA*


* These may be regarded as a satellite-like RNAs as they appear to be essential components of a disease complex.

† These in turn depend upon viruses in the family Luteoviridae for their encapsidation and transmission.

8c Small circular single stranded satellite RNAs

These satellites have genomes that are about 350 nt long. Both circular and linear forms of the genome are found in infected cells. In some cases (e.g. the satellite RNA associated with tobacco ringspot virus, genus Nepovirus), replication involves self-cleavage of circular progeny molecules by an RNA-catalyzed reaction.

List of group members


Satellite RNAs associated with viruses in the familySecoviridae

 Arabis mosaic virus small satellite RNA


 Chicory yellow mottle virus satellite RNA


 Tobacco ringspot virus satellite RNA


Satellite RNAs associated with viruses in the familyLuteoviridae

 Cereal yellow dwarf virus-RPV satellite RNA


Satellite RNAs associated with viruses in the genusSobemovirus

 Lucerne transient streak virus satellite RNA


 Rice yellow mottle virus satellite


 Solanum nodiflorum mottle virus satellite RNA


 Subterranean clover mottle virus satellite RNA (2 types)


 Velvet tobacco mottle virus satellite RNA


Possible member


 Cherry small circular viroid-like RNA



8d Hepadnavirus-associated satellite-like RNAs (Deltavirus)

Hepatitis D virus (HDV, genus Deltavirus) has a single molecule of circular, negative sense 1.7 kb ssRNA that encodes a 24 kDa small protein (S-HDAg) and a 27 kDa large protein (L-HDAg). The ribonucleoprotein of HDV RNA and both HDAgs, are packaged within an envelope containing lipid and helper virus antigens. For complete replication and transmission, HDV also requires a host DNA dependent RNA polymerase II and HBsAg, a protein encoded by its helper virus, human hepatitis B virus (genus Orthohepadnavirus). HDV RNA is encapsidated in distinct virions by the HBsAg capsid protein of the helper virus. HDV is a serious human pathogen and has until now been classified as a virus, although it meets the definitions of a satellite-like RNA. For more details see the chapter on genus Deltavirus.

List of group members

See chapter for genus Deltavirus.

8e Polerovirus-associated RNAs

These ssRNA genomes are about 2.8–3 kb long and have two major ORFs. It is likely that the second ORF, which contains the classic RdRp motifs of the carmovirus supergroup, is translated by readthrough of the ORF1 amber stop codon. Additional small ORFs have been identified in some members. The RNA is capable of autonomous replication but appears to depend on a virus of the genus Polerovirus as helper virus for aphid transmission by encapsidating this RNA with the polerovirus coat protein to form aphid-transmissible hybrid virions. Some members increase the severity of disease symptoms.

List of group members


Beet western yellows virus ST9-associated RNA



Carrot red leaf virus-associated RNA



Tobacco vein distorting virus-associated RNA





Subviral RNA database:

Further reading


Bruening, G. (2001). Virus-dependent RNA agents. In Encyclopedia of Plant Pathology. O. Maloy and T. Murray (eds). Vol. 2: 1170-1177. John Wiley and Sons, New York.

1. Chronic bee-paralysis virus-associated satellite virus

Overton, H.A., Buck, K.W., Bailey, L., Ball, B.V. (1982). Relationships between the RNA components of Chronic bee-paralysis virus and those of Chronic bee-paralysis virus associate. Journal of General Virology 63, 171-179.

Ribière, M., Olivier, V., Blanchard, P. (2010). Chronic bee paralysis: A disease and a virus like no other? Journal of Invertebrate Pathology 103, S120-S131.

2. Satellites that resemble tobacco necrosis satellite virus

Ban, N., Larson, S.B., McPherson, A. (1995). Structural comparison of the plant satellite viruses. Virology, 214, 571-583.

Bringloe, D.H., Gultyaev, A.P., Pelpel, M., Pleij, C.W., Coutts, R.H. (1998). The nucleotide sequence of satellite tobacco necrosis virus strain C and helper-assisted replication of wild-type and mutant clones of the virus. Journal of General Virology 79, 1539-1546.

Dodds, J.A. (1999). Satellite tobacco mosaic virus. Current Topics in Microbiology and Immunology 239, 145-147.

Masuta, C., Zuidema, D., Hunter, B.G., Heaton, L.A., Sopher, D.S., Jackson, A.O. (1987). Analysis of the genome of satellite panicum mosaic virus. Virology, 159, 329-338.

Mirkov, T.E., Mathews, D.M., du Plessis, D.H., Dodds, J.A. (1989). Nucleotide sequence and translation of satellite tobacco mosaic virus RNA. Virology, 170, 139-146.

Qi, D., Omarov, R.T., Scholthof, K.-B.G. (2008). The complex subcellular distribution of satellite panicum mosaic virus capsid protein reflects its multifunctional role during infection. Virology 376, 154-164.

Scholthof, K.-B.G. (1999). A synergism induced by satellite panicum mosaic virus. Molecular Plant-Microbe Interaction 12, 163-166.

Scholthof, K.-B.G., Jones, R.W., Jackson, A.O. (1999). Biology and structure of plant satellite viruses activated by icosahedral helper viruses. Current Topics in Microbiology and Immunology 239, 123-143.

Zhang, L., Zitter, T.A., Palukaitis, P. (1991). Helper virus-dependent replication, nucleotide sequence and genome organization of the satellite virus of maize white line mosaic virus. Virology 180, 467-473.

3. Nodavirus-associated satellite virus

Owens, L., La Fauce, K., Juntunen, K., Hayakijkosol, O., Zeng, C. (2009) Macrobrachium rosenbergii nodavirus disease (white tail disease) in Australia. Diseases of Aquatic Organisms 85, 175-180.

Sri Widada, J., Bonami, J.-R. (2004). Characteristics of the monocistronic genome of extra small virus, a virus-like particle associated with Macrobrachium rosenbergii nodavirus: possible candidate for a new species of satellite virus. Journal of General Virology 85, 643-646.

Sudhakaran, R., Syed Musthaq, S., Rajesh Kumar, S., Sarathl, M., Sahul Hameed, A. S. (2008). Cloning and sequencing of capsid protein of Indian isolate of extra small virus from Macrobrachium rosenbergii. Virus Research 131, 283-287.

5. Mimivirus-associated satellite virus (Sputnik, virophage)

Claverie, J. M., Abergel, C. (2009). Mimivirus and its virophage. Annual Review of Genetics 43, 49-66.

La Scola B., Desnues, C., Pagnier, I., Robert, C., Barrassi, L., Fournous, G., Merchat, M., Suzan-Monti, M., Forterre, P., Koonin, E., Raoult, D. (2008). The virophage as a unique parasite of the giant mimivirus. Nature 455,100-104.

Sun, S., La Scola, B., Bowman, V.D., Ryan, C.M., Whitelegge, J.P., Raoult, D., Rossmann, M. G. (2010). Structural studies of the Sputnik virophage. Journal of Virology 84, 894-897.

6a. Alphasatellites

Briddon, R.W., Bull, S.E., Amin, I., Mansoor, S., Bedford, I.D., Rishi, N., Siwatch, S.S., Zafar, M.Y., Abdel-Salam, A.M., Markham, P.G. (2004). Diversity of DNA 1: a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology 324, 462-474.

Gronenborn, B. (2004). Nanoviruses: genome organisation and protein function. Veterinary Microbiology 98, 103-110.

Horser, C.L., Karan, M., Harding, R.M., Dale, J.L. (2001). Additional rep-encoding DNAs associated with banana bunchy top virus. Archives of Virology 146, 71-86.

Paprotka, T., Metzler, V., Jeske, H. (2010). The first DNA 1-like α satellites in association with New World begomoviruses in natural infections. Virology 404, 148-157.

Mansoor, S., Khan, S.H., Bashir, A., Saeed, M., Zafar, Y., Malik, K.A., Briddon, R.W., Stanley, J., Markham, P.G. (1999). Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology, 259, 190-199.

Nawaz-ul-Rehman, M.S., Nahid, N., Mansoor, S., Briddon, R.W., Fauquet, C.M. (2010). Post-transcriptional gene silencing suppressor activity of two non-pathogenic alphasatellites associated with a begomovirus. Virology 405, 300-308.

Saunders, K., Stanley, J. (1999). A nanovirus-like DNA component associated with yellow vein disease of Ageratum conyzoides: evidence for interfamilial recombination between plant DNA viruses. Virology 264, 142-152.

Timchenko, T., Katul, L., Sano, Y., de Kouchkovsky, F., Vetten, H.J., Gronenborn, B. (2000). The master Rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. Virology 274, 189-195.

Timchenko, T., de Kouchkovsky, F., Katul, L., David, D., Vetten, H.J., Gronenborn, D. B. (1999). A single Rep protein initiates replication of multiple genome components of Faba bean necrotic yellows virus, a single-stranded DNA virus of plants. Journal of Virology 73, 10173-10182.

Wu, P.-J., Zhou, X.-P. (2005). Interaction between a nanovirus-like component and the Tobacco curly shoot virus/satellite complex. Acta Biochimica et Biophysica Sinica 37, 25-31.

6b. Betasatellites

Dry, I.B., Krake, L.R., Rigden, J.E., Rezaian, M.A. (1997). A novel subviral agent associated with a geminivirus: the first report of a DNA satellite. Proceedings of the National Academy of Sciences USA 94, 7088-7093.

Briddon, R.W., Brown, J.K., Moriones, E., Stanley, J., Zerbini, M., Zhou, X., Fauquet, C.M. (2008). Recommendations for the classification and nomenclature of the DNA-ß satellites of begomoviruses. Archives of Virology, 153, 763-781.

Briddon, R.W., Bull, S.E., Amin, I., Idris, A.M., Mansoor, S., Bedford, I.D., Dhawan, P., Rishi, N., Siwatch, S.S., Abdel-Salam, A.M., Brown, J.K., Zafar, Y., Markham, P.G. (2003). Diversity of DNA β: a satellite molecule associated with some monopartite begomoviruses. Virology 312, 106-121.

Briddon, R.W., Mansoor, S., Bedford, I.D., Pinner, M.S., Saunders, K., Stanley, J., Zafar, Y., Malik, K.A., Markham, P.G. (2001). Identification of DNA components required for induction of cotton leaf curl disease. Virology 285, 234-243.

Briddon, R.W., Stanley, J. (2006). Sub-viral agents associated with plant single-stranded DNA viruses. Virology 344, 198-210.

Cui, X., Li, G., Wang, D., Hu, D., Zhou, X. (2005). A begomovirus DNA β-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. Journal of Virology 79, 10764-10775.

Mansoor, S. Briddon, R.W., Zafar, Y., Stanley, J. (2003). Geminivirus disease complexes: an emerging threat. Trends in Plant Sciences 8, 128-134.

Nawaz-ul-Rehman, M.S., Mansoor, S., Briddon, R.W., Fauquet, C.M. (2009). Maintenance of an Old World betasatellite by a New World helper begomovirus and possible rapid adaptation of the betasatellite. Journal of Virology 83, 9347-9355.

Saeed, S., Zafar, Y., Randles, J.W., Rezaian, M.A. (2007). A monopartite begomovirus-associated DNA β satellite substitutes for the DNA B of a bipartite begomovirus to permit systemic infection. Journal of General Virology 88, 2881-2889.

Saunders, K., Bedford, I.D., Briddon, R.W., Markham, P.G., Wong, S.M., Stanley, J. (2000). A unique virus complex causes Ageratum yellow vein disease. Proceedings of the National Academy of Sciences USA 97, 6890-6895.

Saunders, K., Briddon, R. W., Stanley, J. (2008). Replication promiscuity of DNA-β satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-β satellite localizes sequences involved in replication. Journal of General Virology 89, 3165-3172.

Saunders, K., Norman, A., Gucciardo, S., Stanley, J. (2004). The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1). Virology 324, 37-47.

Yang, J.-Y., Iwasaki, M., Machida, C., Machida, Y., Zhou, X., Chua, N.-H. (2008). βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes and Development 22, 2564-2577.

Zhou, X., Xie, Y., Tao, X., Zhang, Z., Li, Z., Fauquet, C.M. (2003). Characterization of DNA β associated with begomoviruses in China and evidence for co-evolution with their cognate viral DNA-A. Journal of General Virology 84, 237-247.

7. Double-stranded satellite RNAs

Ghabrial, S.A., Ochao, W., Baker, T.B., Nibert, M. (2008). Partitiviruses: General features. In: Mahy, B. W. J., Van Regenmortel M., H. V. (Eds.), Encyclopedia of Virology, 3rd edn, vol. 4. Elsevier, Oxford, pp. 68-75.

Kotani,E., Hayashi,Y., Sugimura,Y., Furusawa,T. (2005). Identification of novel

double-stranded RNA produced in Midgut epithelial tissue of the silkworm, Bombyx mori, during Infection by a cypovirus 1. Journal of Insect Biotechnology and Sericology 74, 29-34.

Schmitt, M.J., Breinig, F. (2006). Yeast viral killer toxin: Lethality and self protection. Nature Reviews Microbiology 4, 212-221.

Shelbourn, S.L., Day, P.R., Buck, K.W. (1988). Relationships and functions of virus double-stranded RNA in a P4 killer strain of Ustilago maydis. Journal of General Virology 69, 975-982.

Tai, J.-H., Chang, S.-C., Ip, C.-F., Ong, S.-J. (1995). Identification of a satellite double-stranded RNA in the parasitic protozoan Trichomonas vaginalis infected with T. vaginalis virus T1. Virology 208, 189-196.

Wickner, R.B. (1996). Double-stranded RNA viruses of Saccharomyces cerevisiae. Microbiology Reviews 60, 250-265.

8a. Large linear single-stranded satellite RNAs

Fritsch, C., Mayo, M.A., Hemmer, O. (1993). Properties of satellite RNA of nepoviruses. Biochimie 75, 561-567.

Hans, F., Pinck, M., Pinck, L. (1993). Location of the replication determinants of the satellite RNA associated with grapevine fanleaf nepovirus (strain F13). Biochimie 75, 597-603.

Hemmer, O., Meyer, M., Greif, C., Fritsch, C. (1987). Comparison of the nucleotide sequences of five tomato black ring virus satellite RNAs. Journal of General Virology 68, 1823-1833.

Kigachi, T., Saito, M., Tamada, T. (1996). Nucleotide sequence analysis of RNA-5 of five isolates of beet necrotic yellow vein virus and the identity of a deletion mutant. Journal of General Virology 77, 575-580.

Kreiah, S., Cooper, J.I., Strunk, G. (1993). The nucleotide sequence of a satellite RNA associated with strawberry latent ringspot virus. Journal of General Virology 74, 1163-1165.

Lin, N.S., Lee, Y.S., Lin, B.Y., Lee, C.W., Hsu, Y.H. (1996). The open reading frame of bamboo mosaic potexvirus satellite RNA is not essential for its replication and can be replaced with a bacterial gene. Proceedings of the National Academy of Sciences USA 93, 3138-3142.

Liu, Y.Y., Cooper, J.I. (1993). The multiplication in plants of arabis mosaic virus satellite RNA requires the encoded protein. Journal of General Virology 74, 1471-1474.

Mayo, M.A., Taliansky, M.E., Fritsch, C. (1999). Large satellite RNA: Molecular parasitism or molecular symbiosis. Current Topics in Microbiology and Immunology 239, 65-79.

Rubino, L., Tousignant, M.E., Steger, G., Kaper, J.M. (1990). Nucleotide sequence and structural analysis of two satellite RNAs associated with chicory yellow mottle virus. Journal of General Virology 71, 1897-1903.

8b. Small linear single-stranded satellite and satellite-like RNAs

Cabrera, O., Scholthof, K.-B.G. (1999). The complex viral etiology of St. Augustine decline. Plant Disease 83, 902-904.

Celix, A., Rodriguez-Cerezo, E., Garcia-Arenal, F. (1997). New satellite RNAs, but no DI RNAs, are found in natural populations of tomato bushy stunt tombusvirus. Virology 239, 277-284.

Dalmay, T., Rubino, L. (1995). Replication of cymbidium ringspot virus satellite RNA mutants. Virology 206, 1092-1098.

Demler, S.A., de Zoeten, G.A. (1989). Characterization of a small satellite RNA associated with pea enation mosaic virus. Journal of General Virology 70, 1075-1084.

Francki, R.I.B. (1985). Plant virus satellites. Annual Review of Microbiology 39, 151-174.

Gallitelli, D., Hull, R. (1985). Characterization of satellite RNAs associated with tomato bushy stunt virus and five other definitive tombusviruses. Journal of General Virology 66, 1533-1543.

García-Arenal, F., Palukaitis, P. (1999). Structure and functional relationships of satellite RNAs of Cucumber mosaic virus. Current Topics in Microbiology and Immunology 239, 37-63.

Guo, L-H., Cao, Y-H., Li, D-W., Niu, S-N., Cai, Z-N., Han, C-G., Zhai, Y-F., Yu, J-L. (2005). Analysis of nucleotide sequence and multimeric forms of a novel satellite RNA associated with black beet scorch virus. Journal of Virology 79, 3664-3674.

Menzel, W., Maiss, E., Vetten, H.J. (2009). Nucleotide sequence of a satellite RNA associated with carrot motley dwarf in parsley and carrot. Virus Genes 38, 187-188.

Naidu, R.A, Collins, G.B., Ghabrial, S.A. (1992). Peanut stunt virus satellite RNA: analysis of sequences that affect symptom attenuation in tobacco. Virology 189, 668-677.

Rubino, L., Russo, M. (2010). Properties of a novel satellite RNA associated with tomato bushy stunt virus. Journal of General Virology 91, 2393-2401.

Simon, A.E. (1999). Replication, recombination, and symptom-modulation properties of the satellite RNAs of turnip crinkle virus. Current Topics in Microbiology and Immunology 239, 19-36.

Simon, A.E., Howell, S.H. (1986). The virulent satellite RNA of turnip crinkle virus has a major domain homologous to the 3’ end of the helper virus genome. EMBO Journal 5, 3423-3428.

8c. Small circular single-stranded satellite RNAs

AbouHaidar, M.G., Paliwal, Y.C. (1988). Comparison of the nucleotide sequences of viroid-like satellite RNA of the Canadian and Australasian strains of lucerne transient streak virus. Journal of General Virology 69, 2369-2373.

Davies, C., Haseloff, J., Symons, R.H. (1990). Structure, self-cleavage, and replication of two viroid-like satellite RNAs (virusoids) of subterranean clover mottle virus. Virology 177, 216-224.

Etscheid, M., Tousignant, M.E., Kaper, J.M. (1995). Small satellite of arabis mosaic virus autolytic processing of in vitro transcripts of (+) and (-) polarity and infectivity of (+) strand transcripts. Journal of General Virology 76, 271-282.

Passmore, B.K., Bruening, G. (1993). Similar structure and reactivity of satellite tobacco ringspot virus RNA obtained from infected tissue and by in vitro transcription. Virology 197, 108-115.

Rasochova, L., Miller, W.A. (1996). Satellite RNA of barley yellow dwarf-RPV virus reduces accumulation of RPV helper virus RNA and attenuates RPV symptoms in oats. Molecular Plant-Microbe Interactions 9, 646-650.

Rubino, L., Tousignant, M.E., Steger, G., Kaper, J.M. (1990). Nucleotide sequence and structural analysis of two satellite RNAs associated with chicory yellow mottle virus. Journal of General Virology 71, 1897-1903.

Sehgal, O.P., AbouHaidar, M.G., Gellatly, D.L., Ivanov, I., Thottapilly, G. (1993). An associated small RNA in rice yellow mottle sobemovirus homologous to the satellite RNA of lucerne transient streak sobemovirus. Phytopathology 83, 1309-1311.

Symons, R.H. (1997). Plant pathogenic RNAs and RNA catalysis. Nucleic Acids Research 25, 2683-2689.

Symons, R.H., Randles, J.W. (1999). Encapsidated circular viroid-like satellite RNAs. Current Topics in Microbiology and Immunology 239, 81-105.

8e. Polerovirus-associated RNAs

Chin L.-S., Foster J., Falk B.W. (1993). The beet western yellows virus ST9-associated RNA shares structural and nucleotide sequence with the carmo-like viruses. Virology 192, 473-482.

Falk B. W., Duffus J.E. (1984). Identification of small single- and double-stranded RNAs associated with severe symptoms in beet western yellows virus-infected Capsella bursa-pastoris. Phytopathology 74, 1224-1229.

Mo X.-H., Chen, Z.-B., Chen, J.-P. (2011). Molecular identification and phylogenetic analysis of a viral RNA associated with the Chinese tobacco bushy top disease complex. Annals of Applied Biology, in press.

Passmore B.K., Sanger M., Chin L.-S., Falk B.W., Bruening, G. (1993). A subviral, independently-replicating RNA stimulates the replication of beet western yellows luteovirus. Proceedings of the National Academy of Sciences of the USA 90, 10168-10172.

Sanger M., Passmore B., Falk B W., Bruening G., Ding B., Lucas W J. (1994). Symptom severity of beet western yellows virus stain ST9 is conferred by the associated RNA and is not associated with virus release from the phloem. Virology 200, 48-55.

Watson M.T., Tian T.Y., Estabrook E., Falk B.W. (1998). A small RNA resembling the beet western yellows luteovirus ST9-associated RNA is a component of the California carrot motley dwarf complex. Phytopathology 88, 164-170.

Contributed by

Briddon, R.W., Ghabrial, S., Lin, N.-S., Palukaitis, P., Scholthof, K.-B.G. and Vetten, H.-J.