Lily mottle virus

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Lily mottle virus
Virus classification OOjs UI icon edit-ltr.svg
(unranked): Virus
Realm: Riboviria
Kingdom: Orthornavirae
Phylum: Pisuviricota
Class: Stelpaviricetes
Order: Patatavirales
Family: Potyviridae
Genus: Potyvirus
Species:
Lily mottle virus

The Lily mottle virus (LMoV), is a plant virus of the Potyviridae virus family that causes asymptomatic to mild diseases of individual plant parts in plants of the lily family ( Liliaceae ). However, a frequently occurring simultaneous infection with other plant viruses, which on their own only cause moderate or no disease, can cause the entire plant to perish. This coinfection leads to considerable crop damage in lily cultivation and is therefore of great economic importance. Lily mottle virus is spread by aphids and in horticulture during vegetative propagation by splitting the lily bulb. LMoV was regarded as a synonym for a subtype of the Tulip Breaking Virus (TBV) that occurs in lilies, although since 2005 it has been classified as a closely related but independent virus species of the genus Potyvirus .

Contents

Discovery

The symptoms of the plant disease caused by LMoV were already known in the 19th century. Yet it was not until 1944 that P. Brierley and F. F. Smith succeeded in proving a coinfection with two viruses as the cause through infection experiments on several tulip and lily species. [1] They were able to detect the Lily symptomless virus (LSV, order Tymovirales : Betaflexiviridae : Carlavirus ) in several lily species grown in the USA ( Lilium auratum , L. speciosum , L. longiflorum ), which showed streaky brightening (chlorosis) or individual necrotic spots on the leaves, which was always present simultaneously with the Cucumber mosaic virus (CMV) or the Lily mottle virus. [2] They were also able to demonstrate that all three viruses are transmitted by aphids of the species Aphis gossypii .

Virus structure

Morphology

Virus particles (virions) of the Lily mottle virus consist of a thread-like capsid with helical symmetry, in which a single-stranded RNA is packed as a genome; a viral envelope is not present. [3] The capsid is 13 nm thick and about 740 nm long. The length of the capsid increases in the presence of divalent cations (especially calcium ions) in the preparation and decreases after binding by the addition of EDTA. The individual capsomeres that make up the capsid require a pitch of 3.4 nm for one helix turn. Compared to viruses with rigid rods and a comparable structure (e.g. the Tobacco mosaic virus- TMV), this duct height is relatively large and enables the LMoV capsid to be flexible and bendable. One turn requires 7.7 capsomeres, so that the entire capsid is composed of about 1700 capsomeres. [4] The individual capsomeres consist of only one molecule of the LMoV capsid protein (CP, coat/capsid protein) with a length of 274 amino acids (33 kDa). The CP is folded several times in such a way that the N- and C-terminus point outwards. These outer ends of the capsid protein are very variable. The protruding N-terminus mainly determines the specific attachment to the host cell and enables the serological differentiation of different virus isolates. The highly conserved sections in the middle of the CP (216 amino acids) within the different members of the Potyviridae point inwards in the capsid and interact with the viral RNA. [5]

Schematic structure of the LMoV capsid (section with eight helix turns). Conserved areas of the capsid protein (gray), N-terminus (blue) and C-terminus (red) LMoV-Kapsid.png
Schematic structure of the LMoV capsid (section with eight helix turns). Conserved areas of the capsid protein (gray), N-terminus (blue) and C-terminus (red)

The virions are stable against ethanol and lose their infectivity in the plant sap only after 10 minutes at 65-70 °C. [1] The LMoV has a density of 1.31 g/ml in density gradient centrifugation (caesium chloride) and a sedimentation rate of 137 to 160 S. [6]

Genome

The genome of LMoV is a linear, single-stranded RNA with positive polarity [(+)ssRNA] and a length of 9644 nucleotides. A viral protein (VPg) is covalently bound to the 5'-end of the RNA. As with cellular messenger RNAs, a poly(A) tail of 20 to 160 adenosines is located at the 3' end of the viral genome. Between the two non-coding ends (NCR: non-coding region) is an open reading frame (ORF), which codes for a polyprotein of 3095 amino acids. This polyprotein is cleaved into the individual viral proteins by proteases during translation.

An IRES structure was suspected in the 5'-NCR of potyviruses, as translation is initiated without a 5'-cap structure. [7] LMoV does not have a cap structure, nor could an IRES be confirmed from sequence data. The VPg protein bound to the 5'-NCR possibly serves as a primer for the RNA polymerase to amplify the RNA. However, the VPg of other potyviruses also interacts directly with the translation initiation factors eIF4E and eIFiso4E. [8] This could represent an as yet uncharacterized, Cap- and IRES-independent translation pathway. [9]

Virus proteins and replication

After infection, the virus enters the plant via the vascular bundle and is taken up by the cells through membrane vesicles (endocytosis). In the cytoplasm, the capsid disintegrates and the RNA is released. The viral RNA can also enter the cell very effectively via infected neighboring cells through cell contact sites (plasmodesmata). This direct transport of naked, infectious RNA is controlled by several viral proteins, including the so-called HC (helper component), which form a so-called movement complex. As with all (+)ssRNA viruses, the ingested RNA is first translated into protein at the ribosomes, as at least one copy of the viral RNA-dependent RNA polymerase is required for the replication of the RNA. After this has synthesized several copies of the viral RNA, the LMoV proteins are produced in large quantities. These accumulate at the synthesis sites of the viroplasm to form morphologically visible inclusion bodies. When infected with LMoV, these inclusion bodies have a characteristic, cylindrical to spiral-like shape in the cytoplasm; the virus protein that predominantly forms these cylinders is therefore also referred to as CI (cylindrical inclusion). Amorphous inclusion bodies are formed in the cell nucleus, which consist of two viral proteins NIa and NIb (nuclear inclusions). As the viral proteins are always formed in the same ratio during translation of the RNA and larger quantities of the capsid protein are required in comparison to other proteins, these proteins, which are not required in many copies, form inclusion bodies, are degraded or excreted from the cell.

Genome organization of LMoV: P1(protease 1), HC (helper component), P3 (protease 3), CI (cylindrical inclusions protein), VPg (genomic virus protein), Pro (protease), NI (nuclear inclusions protein), CP(capsid/coat protein). The interfaces of the proteases are shown as wedges. LMoV-Genomkarte.jpg
Genome organization of LMoV: P1( protease 1), HC ( helper component), P3 (protease 3), CI ( cylindrical inclusions protein), VPg (genomic virus protein), Pro (protease), NI ( nuclear inclusions protein), CP( capsid/coat protein). The interfaces of the proteases are shown as wedges.

The LMoV polyprotein is cleaved into eight individual proteins by viral proteases. At the N-terminus, viral protease 1 (P1) cleaves itself from the polyprotein. Next comes the HC protein, which is important for transmission by aphids; however, the mechanism is unclear. The HC has a papain-like protein domain at the C-terminus, with which the HC also splits off independently from the polyprotein. All other proteins are cleaved by the NIa protease. This is followed by a further protease (P3) with an as yet unknown function and the CI, from which a small peptide 6K1 is cleaved (possibly for activation). The CI is active as a helicase during RNA replication. Together with a protease component, the VPg forms the NIa. The NIb is the viral RNA polymerase from which the viral capsid protein CP is cleaved. Once sufficient viral (+)ssRNA and CP have been formed, packaging into the capsid can take place and mature viruses can be released into the plant sap by exocytosis. The much more effective infection of the naked RNA from cell to cell explains the appearance of patchy lesions on the leaves.

Classification

The genus Potyvirus is currently the largest group of all plant viruses with 168 virus species. [10] This large number of Potyviruses makes it difficult to distinguish and delimit individual species or subtypes, especially the Lily mottle virus and the Tulip breaking virus (TBV), which were long considered synonyms of a single species. LMoV was regarded as the subtype of TBV (TBV subtype Lily) that was widespread in lilies. This distinction was made even more complex by the fact that the true species TBV can also cause disease in lilies. With more and more comparative sequences of the genome of different virus isolates, incorrect assignments have so far been detected. [11] In a study of 187 complete genome sequences and 1220 partial sequences for the capsid protein of potyviruses, several subgroups within the genus were identified and the criteria for the species limits were also redefined for LMoV and TBV. [12] Accordingly, a match in the nucleotide sequence between two complete genomes of more than 76% is considered a species limit (corresponds to 82% match in the amino acid sequence). The part of the nucleotide sequence coding for the capsid protein CP showed a species limit of 76-77%. The sequence of the CI protein appeared to be the most suitable for differentiation. Several sequences of potyviruses (including TBV and LMoV), which were published in the international gene bank GenBank, had to be assigned to other species as a result.

The taxonomy defined by the "International Committee on Taxonomy of Viruses" and valid since 2005 includes subtypes of LMoV previously classified as TBV: [13]

  • Family Potyviridae
  • Genus Potyvirus
  • Species Lily-Mottle-Virus (LMoV)
  • Subtype Lily-Mild-Mottle-Virus
  • Subtype Lily-Mottle-Virus
  • Subtype Tulip-band-breaking-Virus
  • Subtype Mild tulip breaking virus (MTBV) [14]
  • Subtype Severe tulip breaking virus (STBV) [14]

Infection and disease caused by LMoV

About two weeks after being infected with LMoV, a light green mottle appears on young leaves. The discoloration can also appear in stripes along the leaf veins. Over the course of a few days, the leaf becomes thinner in the light spots and in severe cases the plant cells can die in these areas; the irregularly defined spots now appear dark brown and dried out. All new shoots and flowers that sprout after infection are reduced in size and often deformed.

However, the severity of the disease symptoms varies greatly between different lily species and hybrids. Even the disease of identical species in a single cultivation area varies in severity. This phenomenon can be explained by the influence of the growth phase at the time of infection, the point of entry and the infectious dose of the virus. In the Easter lily ( L. longiflorum ), no disease regularly develops, although the virus multiplies in the plant. In the tiger lily ( L. lancifolium ), only a very slight light green mottling occurs. In some LMoV infections, only reduced length growth and smaller flowers and bulbs can be observed. The economically important species L. formosanum always falls ill after an LMoV infection; this also applies to the wild varieties found in Taiwan. Only the specially selected variety Lilium formosanum "Little Snow White" has increased virus resistance. Very susceptible to LMoV and other plant viruses found in lilies is the hybrid "Enchantment" bred by Jan de Graaff in 1941 and all cultivars derived from it, such as the cultivar Lilium Asia . Hybrid cv. Enchantment. [11]

Infection with LMoV alone never leads to the death of the entire plant, but remains locally limited to some parts of the plant. However, a coinfection of LMoV with the Lily symptomless virus is particularly common, which alone does not cause any symptoms of the disease, but only reduced plant growth. If a plant is infected by both viruses, the disease progresses much more severely and quickly. After the initial typical symptoms of a pronounced LMoV infection, larger vascular bundles such as the entire phloem are affected, which ultimately causes the entire plant to die. A double-infected lily bulb can already be severely damaged during storage, lose its ability to sprout and die.

Transmission and spread

Transmission

Reed aphids ingesting plant sap]] The Lily Mottle virus is transmitted during the feeding act of aphids (Aphididae). The aphids ingest the virus, which is present in high concentrations in the plant sap, during the feeding act and can infect other plants with a delay of a few hours. The virus cannot multiply in the aphid itself. After absorption of the plant sap into the aphid's midgut, the virus is distributed in the bloodstream and enters the saliva of the sucking apparatus; a new plant can then be infected during the next feeding. The aphid species that predominantly transmit LMoV are Aphis gossypii , Myzus persicae , Macrosiphum euphorbiae and Doralis fabae . Stored bulbs can also be infected with the virus by Anuraphis (Yezabura) tulipae . [15] Winged specimens of the aphid population enable transmission over long distances.

Reed aphids ingesting plant sap Aphidoidea puceron Luc Viatour.jpg
Reed aphids ingesting plant sap

During plant cultivation, the virus is transmitted when the plants are cut and injured with contaminated knives and scissors. Experimentally, this route of infection is used by targeted scoring of the plants. Splitting the lily bulbs during vegetative propagation spreads the virus to all daughter plants. The same applies to vegetative propagation by cuttings in tissue culture, which is very common in industrial horticulture. The virus is not spread by seeds; if a new plant germinates from the seed of an LMoV-infected plant, it is not infected.

Distribution

Bulb of a Lilium sp. Xant lut bulbus.jpg
Bulb of a Lilium sp.

The natural geographical spread of the virus is not known, as when it was discovered in the US in 1944, it was already being spread by man through the global trade in flowers and bulbs. The cultivation of lilies in large greenhouses and fields as a monoculture particularly favors transmission compared to the natural occurrence of wild plants. The virus is spread worldwide and is endemic in countries with significant lily cultivation. In addition to the United States, this includes the Netherlands, Poland, North and South Korea, Japan, Taiwan, China and Israel. The Lily mild mottle virus, a subtype of LMoV, was detected in 26.3% of all plants in a study of 185 lily samples from South Korean crops, and a co-infection of LMoV and the Tomato ringspot virus was observed in a further 23.2%. [16]

In the Netherlands, LMoV was detected several times in all plants of individual lily fields of the cultivar "Enchantment". [17] Often there was also an infection with the Lily symptomless virus. In plantations affected in this way, necrosis of the stem and leaves is increasingly observed, which is usually followed by the death of the plant. If all the lilies in a plantation are only infected with LMoV, this does not usually result in the loss of the entire flower crop; smaller flowers or plants with reduced growth are then offered at lower prices.

LMoV was detected in all of the approximately 340 lily cultivars grown on a large scale. [18] The undetected spread through worldwide transportation is particularly prevalent in those lily species that show no or only minor symptoms of infection, but can propagate the virus, such as the Easter lily and Tiger lily. The virus has a wider host range than was assumed in earlier studies. For example, LMoV was also detected in the winter endive (C. endivia L. var. latifolium Lam.). [19]

Prevention of the infection

The spread of LMoV in industrial production is primarily prevented by controlling the aphids as carriers. [18] The virus is mainly transmitted by spreading aphid populations in June and July, less so in May and August. Weekly control of the insects from May and biweekly in August and September is carried out on an industrial scale. The lilies are most often treated with kerosene oil or pyrethroids as aerosols.

To prevent infection, it is important to avoid further spread through seed bulbs and the global plant trade. Those lily species with no or only mild symptoms are a particular source of infection outbreaks, as the infection remains undetected. For this reason, the simultaneous cultivation of resistant and susceptible lily varieties is often avoided, as the virus can spread unnoticed in the resistant varieties without developing disease symptoms. These form a permanent reservoir for the infection of the susceptible varieties. In a monoculture of susceptible varieties, infected plants can be sorted out and thus the spread of the virus can be controlled to a certain extent. As the virus is not transmitted by seed like other members of the Potyvirus genus, a crop can be freed from infection with LMoV by more complex, renewed breeding from seed.

The transportation and trade of plant parts such as flowers, cuttings or bulbs from cultivation areas in which LMoV has been detected is subject to legal restrictions or an import ban in many countries. In particular, plant parts traded for propagation and breeding have had to be tested for LMoV in Germany since 1998 in accordance with the implementation of several EU directives. [20] To detect LMoV, immunological tests for LMoV virus proteins (ELISA) and, rarely, detection of the virus genome by PCR are used. Both the leaves ("leaf test") and the harvested bulbs ("bulb test") are used as test samples for diagnostics. Newer methods for the simultaneous detection of several plant viruses from one sample by DNA hybridization (macroarray) are currently being tested. [21]

Related Research Articles

<i>Potyviridae</i> Family of viruses

Potyviridae is a family of positive-strand RNA viruses that encompasses more than 30% of known plant viruses, many of which are of great agricultural significance. The family has 12 genera and 235 species, three of which are unassigned to a genus.

<i>Potyvirus</i> Genus of positive-strand RNA viruses in the family Potyviridae

Potyvirus is a genus of positive-strand RNA viruses in the family Potyviridae. Plants serve as natural hosts. Like begomoviruses, members of this genus may cause significant losses in agricultural, pastoral, horticultural, and ornamental crops. More than 200 species of aphids spread potyviruses, and most are from the subfamily Aphidinae. The genus contains 190 species and potyviruses account for about thirty percent of all currently known plant viruses.

<i>Alfalfa mosaic virus</i> Species of virus

Alfalfa mosaic virus (AMV), also known as Lucerne mosaic virus or Potato calico virus, is a worldwide distributed phytopathogen that can lead to necrosis and yellow mosaics on a large variety of plant species, including commercially important crops. It is the only Alfamovirus of the family Bromoviridae. In 1931 Weimer J.L. was the first to report AMV in alfalfa. Transmission of the virus occurs mainly by some aphids, by seeds or by pollen to the seed.

Asparagus virus 1 (AV-1) is one of the nine known viruses that infects asparagus plants. It is a member of the genus Potyvirus in the family Potyviridae. Initially reported by G. L Hein in 1960, it causes no distinct symptoms in asparagus plants. The only known natural plant host is the asparagus. It is spread by aphid vectors, which means that aphids do not cause the AV-1, but they do spread it.

<i>Bidens mottle virus</i> Species of virus

Bidens mottle virus (BiMoV) is a pathogenic plant virus in the plant virus family Potyviridae. BiMoV is a flexuous filamentous particle, 720 nm long, and belongs to the Potyviridae genus Potyvirus. Like other viruses in this genus, Bidens mottle virus is transmitted both mechanically by sap and by aphids in a stylet-borne fashion.

Pepper mottle virus (PepMoV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the Potyvirus genus, PepMV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 737 nm in length. Isolates of this virus has been completely sequenced and its RNA is 9640 nucleotides long. This virus is transmitted by several species of aphids in a nonpersitant manner and by mechanical inoculation.

Potato virus Y (PVY) is a plant pathogenic virus of the family Potyviridae, and one of the most important plant viruses affecting potato production.

<i>Tobacco etch virus</i> Species of virus

Tobacco etch virus (TEV) is a plant virus in the genus Potyvirus and family Potyviridae. Like other members of the genus Potyvirus, TEV has a monopartite positive-sense, single-stranded RNA genome surrounded by a capsid made from a single viral encoded protein. The virus is a filamentous particle that measures about 730 nm in length. It is transmissible in a non-persistent manner by more than 10 species of aphids including Myzus persicae. It also is easily transmitted by mechanical means but is not known to be transmitted by seeds.

Sweet potato feathery mottle virus (SPFMV) is a member of the genus Potyvirus in the family Potyviridae. It is most widely recognized as one of the most regularly occurring causal agents of sweet potato viral disease (SPVD) and is currently observed in every continent except Antarctica. The number of locations where it is found is still increasing; generally, it is assumed that the virus is present wherever its host is. The virus has four strains that are found in varying parts of the world.

<i>Tulip breaking virus</i> Species of virus

Tulip breaking virus is one of five plant viruses of the family Potyviridae that cause color-breaking of tulip flowers. These viruses infect plants in only two genera of the family Liliaceae: tulips (Tulipa) and lilies (Lilium).

Apium virus Y (ApVY) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae.

Commelina mosaic virus (CoMV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the Potyvirus genus, CoMV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 707-808 nm in length. This virus is transmitted by two species of aphids, Myzus persicae and Aphis gossypii, and by mechanical inoculation.

Clover yellow vein virus (ClYVV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the Potyvirus genus, ClYVV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 760 nm in length. This virus is transmitted by several species of aphids in a nonpersistent manner and by mechanical inoculation.

Passion fruit woodiness virus (PWV) is a plant pathogenic virus in the genus Potyvirus and the virus family Potyviridae. Like other members of the genus Potyvirus, PWV is a monopartite strand of positive-sense, single-stranded RNA surrounded by a capsid made for a single viral encoded protein. The virus is a filamentous particle that measures about 745 nm in length.

<i>Watermelon mosaic virus</i> Species of virus

Watermelon mosaic virus (WMV) also known as Marrow mosaic virus, Melon mosaic virus, and until recently Watermelon mosaic virus type 2 (WMV-2), is a plant pathogenic virus that causes viral infection in many different plants. The virus itself is referred to as Watermelon Mosaic Virus II or WMV-2 and is an isolate of the U.S. WMV-2 is a ssRNA positive strand virus that is part of the Potyviridae or Potyvirus clade. Like all RNA viruses, it contains a protein capsid which protects the inner viral RNA. First described on squash in Florida, WMV arose from a unique recombination of genetic material contributed by Soybean mosaic virus (SMV) and Bean common mosaic virus (BCMV) along with Peanut Stripe virus (PSV).

''Narcissus white streak virus (NWSV) is a plant pathogen of the family Potyviridae which infects plants of the genus Narcissus, and is transmitted by aphids. It is among the commonest and most serious of the viral infections that infect narcissi, but appears to be confined to N. tazetta.

Cassava brown streak virus is a species of positive-strand RNA viruses in the genus Ipomovirus and family Potyviridae which infects plants. Member viruses are unique in their induction of pinwheel, or scroll-shaped inclusion bodies in the cytoplasm of infected cells. Cylindrical inclusion bodies include aggregations of virus-encoded helicase proteins. These inclusion bodies are thought to be sites of viral replication and assembly, making then an important factor in the viral lifecycle. Viruses from both the species Cassava brown streak virus and Ugandan cassava brown streak virus (UCBSV), lead to the development of Cassava Brown Streak Disease (CBSD) within cassava plants.

Carrot virus Y (CarVY) is a (+)ss-RNA virus that affects crops of the carrot family (Apiaceae), such as carrots, anise, chervil, coriander, cumin, dill and parsnip. Carrots are the only known crop to be infected in the field. Infection by the virus leads to deformed roots and discolored or mottled leaves. The virus is spread through insect vectors, and is currently only found in Australia.

<i>Onion yellow dwarf virus</i> Species of virus

Onion yellow dwarf virus (OYDV) is a plant virus in the genus Potyvirus that has been identified worldwide and mainly infects species of Allium such as onion, garlic, and leek. The virus causes mild to severe leaf malformation, and bulb reduction up to sixty percent has been observed in garlic.

References

Bibliography

Individual references

  1. 1 2 P. Brierley und F. F. Smith: Studies on lily virus diseases: the necrotic fleck complex of Lilium longiflorum. Phytopathology (1944) 34, S. 529–555.
  2. ↑ Kenneth M. Smith: Virus diseases of farm & garden, 1946, S. 82–83
  3. ↑ E. L. Dekker EL et al.: Characterization of potyviruses from tulip and lily which cause flower-breaking. Journal of General Virology (1993) 74(5), S. 881–887; PMID   8492092
  4. ↑ Drews (2004) S. 149.
  5. ↑ D. D. Shukla und C. W. Ward: Structure of potyvirus coat proteins and its application in the taxonomy of the potyvirus group. Adv. Virus Research (1989) 36, S. 273–314 (Review); PMID   2472047
  6. ↑ Berger (2005) S. 819.
  7. ↑ D. R. Gallie: Cap-independent translation conferred by the 5' leader of tobacco etch virus is eukaryotic initiation factor 4G dependent. Journal of Virology (2001) 75(24), S. 12141–12152; PMID   11711605
  8. ↑ S. Wittmann et al.: Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology (1997) 234, S. 84–92; PMID   9234949
  9. ↑ S. Léonard et al.: Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. Journal of Virology (2000) 74(17), S. 7730–7737; PMID   10933678
  10. ↑ ICTV: Master Species List 2018a v1 (Memento des Originals vom 14. März 2019 im Internet Archive)  Info: Der Archivlink wurde automatisch eingesetzt und noch nicht geprüft. Bitte prüfe Original- und Archivlink gemäß Anleitung und entferne dann diesen Hinweis. MSL including all taxa updates since the 2017 release. Fall 2018 (MSL #33)
  11. 1 2 Y. Yamaji, L. Xiaoyun et al.: Molecular evidence that a lily-infecting strain of Tulip breaking virus from Japan is a strain of lily mottle virus. European Journal of Plant Pathology (2001) 107, 8, S. 833–837 (Abstract)
  12. ↑ M. J. Adams, J. F.Antoniw und C. W. Fauquet: Molecular criteria for genus and species discrimination within the family Potyviridae. Archives of Virology (2005) 150(3), S. 459–479; PMID   15592889
  13. ↑ P. H. Berger (2005) S. 824 und 827.
  14. 1 2 Brunt, A.A., Crabtree, K., Dallwitz, M.J., Gibbs, A.J., Watson, L. and Zurcher, E.J. (Hrsg.): Tulip breaking potyvirus, auf: Plant Viruses Online: Descriptions and Lists from the VIDE Database (1996 onwards). Version: 16th January 1997
  15. ↑ Smith (1972), S. 552.
  16. ↑ K. Lee et al.: Virus disease of Lilies in Korea. Acta Horticulturae (ISHS), International Symposium on the Genus Lilium (1996) 414, S. 195–202.
  17. ↑ Allan Granoff, Robert G. Webster (eds.): Encyclopedia of Virology, San Diego (Academic Press) 1999, Band 2, S. 1321; ISBN   0-12-227030-4
  18. 1 2 C. J. Asjes: Control of aphid-borne Lily symptomless virus and Lily mottle virus in Lilium in the Netherlands. Virus Research (2000) 71(1–2), S. 23–32; PMID   11137159 (Review).
  19. ↑ V. Lisa, H. J. Vetten, D.-E. Lesemann, P. Gotta: Occurrence of Lily mottle virus in escarole. Plant Disease (2002) 86, S. 329
  20. ↑ Verordnung über das Inverkehrbringen von Anbaumaterial von Gemüse-, Obst- und Zierpflanzenarten sowie zur Aufhebung der Verordnung zur Bekämpfung von Viruskrankheiten im Obstbau (16. Juni 1998), (BGBl. I S. 1322)
  21. ↑ S. Sugiyama et al.: A simple, sensitive, specific detection of mixed infection of multiple plant viruses using macroarray and microtube hybridization. J. Virol. Methods. (2008) Sep 12. (Epub) PMID   18760308
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