Luteoviruses

Abstract

Luteoviruses, that is, members of the Luteoviridae family, are plant viruses that can infect a wide range of host plants, including many important crops such as cereals, cucurbits, legumes, potato, sugarbeet and sugar cane. Their icosahedral virions contain a single (+) ribonucleic acid genome in a capsid composed of two structural proteins. They are limited to phloem cells in host plants and are only transmitted by aphids in a circulative and nonpropagative mode with high specificity.

Growing data are accumulating on plant–luteovirus relationships and more particularly on the mechanism developed by the virus to overcome plant defence. The tight interaction between luteoviruses and their aphid vector has also been extensively studied. Information from these studies together with a better understanding of the epidemiology of luteoviruses will help to combat their detrimental effects on crops.

Key Concepts:

  • Luteoviruses have a highly compacted genome and use a diversity of translation mechanisms to express viral proteins.

  • Function of the viral gene products is known, but their plant and aphid partners have not been fully identified.

  • Luteoviruses are confined to phloem tissue, but the causes of their phloem restriction are not completely deciphered.

  • Luteoviruses circulate in the vector aphid's body, without any replication, by crossing the gut and the accessory salivary gland epithelia.

  • Epidemiology of luteoviruses reveals a high complexity of mutual ecological interactions between virus, plant and vector, influenced by multiple biotic and abiotic factors.

  • Control of luteoviral diseases includes cultural practices, insecticidal measures, natural and biotechnological plant resistance and epidemiology‐based forecasting systems.

Keywords: plant virus; genome organisation; aphid transmission; epidemiology; virus control

Figure 1.

Genome organisation and map of the translation products of (a) Barley yellow dwarf virus‐PAV, (b) Potato leafroll virus and (c) Pea enation mosaic virus‐1.

Figure 2.

Purified viral particles of Turnip yellows virus. Courtesy of C Reinbold. Bar, 100 nm.

Figure 3.

Diagram of the route of circulative transmitted luteoviruses through the aphid vector. AG, accessory salivary gland; PG, principal salivary gland. Adapted from FE Gildow, in Smith and Barker .

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References

Ashoub A, Rhode W and Prüfer D (1998) In planta transcription of a second subgenomic RNA increases the complexity of the subgroup 2 luteovirus genome. Nucleic Acids Research 26: 420–426.

Barry JK and Miller WA (2002) A‐1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proceedings of the National Academy of Sciences of the USA 99: 11133–11138.

Baumberger N, Tsai CH, Lie M, Havecker E and Baulcombe DC (2007) The polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Current Biology 17: 1609–1614.

Bencharki B, Boissinot S, Revollon S et al. (2010) Phloem protein partners of Cucurbit aphid borne yellows virus: possible involvement of phloem proteins in virus transmission by aphids. Molecular Plant‐Microbe Interactions 23: 799–810.

Beuve M, Stevens M and Liu HY (2008) Biological and molecular characterization of an American sugarbeet‐infecting Beet western yellows virus isolate. Plant Disease 92: 51–60.

Borer ET, Mitchell CE, Power AG and Seabloom EW (2009) Consumers indirectly increase infection risk in grassland food webs. Proceedings of the National Academy of Sciences of the USA 106: 503–506.

Bortolamiol D, Pazhouhandeh M, Marrocco K, Genschik P and Ziegler‐Graff V (2007) The polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Current Biology 17: 1615–1621.

Brault V, van den Heuvel JF, Verbeek M et al. (1995) Aphid transmission of beet western yellows luteovirus requires the minor capsid read‐through protein P74. EMBO Journal 14: 650–659.

Brault V, Herrbach É and Reinbold C (2007) Electron microscopy studies on luteovirid transmission by aphids. Micron 38: 302–312.

Brault V, Périgon S, Reinbold C et al. (2005) The polerovirus minor capsid protein determines vector specificity and intestinal tropism in the aphid. Journal of Virology 79: 9685–9693.

Brault V, Tanguy S, Reinbold C et al. (2010) Transcriptomic analysis of intestinal genes following acquisition of Pea enation mosaic virus by the pea aphid Acyrthosiphon pisum. Journal of General Virology 91: 802–808.

Bruyère A, Brault V, Ziegler‐Graff V et al. (1997) Effects of mutations in the Beet western yellows virus readthrough protein on its expression and packaging and on virus accumulation, symptoms, and aphid transmission. Virology 230: 323–334.

Chay CA, Gunasinge UB, Dinesh‐Kumar SP, Miller WA and Gray SM (1996) Aphid transmission and systemic plant infection determinants of barley yellow dwarf luteovirus‐PAV are contained in the coat protein readthrough domain and 17‐kDa protein, respectively. Virology 219: 57–65.

Chomic A, Pearson MN, Clover GRG et al. (2010) A generic RT‐PCR assay for the detection of Luteoviridae. Plant Pathology 59: 429–442.

Csorba T, Lózsa R, Hutvágner G and Burgyán J (2010) Polerovirus protein P0 prevents the assembly of small RNA‐containing RISC complexes and leads to degradation of ARGONAUTE1. Plant Journal 62: 463–472.

Dombrovsky A, Glanz E, Pearlsman M, Lachman O and Antignus Y (2010) Characterization of Pepper yellow leaf curl virus, a tentative new Polerovirus species causing a yellowing disease of pepper. Phytoparasitica 38: 477–486.

Dedryver CA, Riault G, Tanguy S et al. (2005) Intra‐specific variation and inheritance of BYDV‐PAV transmission in the aphid Sitobion avenae. European Journal of Plant Pathology 111: 341–354.

Fabre F, Plantegenest M, Mieuzet L et al. (2005) Effects of climate and land use on the occurrence of viruliferous aphids and the epidemiology of barley yellow dwarf disease. Agriculture, Ecosystems & Environment 106: 49–55.

Hall GS, Peters JS, Little DP and Power AG (2010) Plant community diversity influences vector behaviour and Barley yellow dwarf virus population structure. Plant Pathology 59: 1152–1158.

Hauser S, Weber C, Vetter G et al. (2000) Improved detection and differentiation of beet polerovirus species by restriction fragment length polymorphism (RFLP), single strand conformation polymorphism (SSCP) and multiplex RT‐PCR. Journal of Virological Methods 89: 11–21.

Hodge S and Powell G (2010) Conditional facilitation of an aphid vector, Acyrthosiphon pisum, by the plant pathogen, Pea enation mosaic virus. Journal of Insect Science 10: 155.

ICTV (2009) Virus Taxonomy: 2009 Release. Available at http://www.ictvonline.org/virusTaxonomy.asp?version=2009. Retrieved on October 2010.

Jaag HM, Kawchuk L, Rohde W et al. (2003) An unusual internal ribosomal entry site of inverted symmetry directs expression of a potato leafroll polerovirus replication‐associated protein. Proceedings of the National Academy of Sciences of the USA 100: 8939–8944.

Knierim D, Deng TC, Tsai WS, Green SK and Kenyon L (2010) Molecular identification of three distinct Polerovirus species and a recombinant Cucurbit aphid‐borne yellows virus strain infecting cucurbit crops in Taiwan. Plant Pathology 59: 991–1002.

Kozlowska‐Makulska A, Guilley H, Szyndel MS et al. (2010) P0 proteins of European beet‐infecting poleroviruses display variable RNA silencing suppression activity. Journal of General Virology 91: 1082–1091.

Lapierre H and Signoret PA (eds) (2004) Viruses and Virus Diseases of Poaceae (Graminae), p. 857 Paris: INRA Editions.

Lee L, Palukaitis P and Gray SM (2002) Host‐dependent requirement for the Potato leafroll virus 17‐kDa protein in virus movement. Molecular Plant‐Microbe Interactions 15: 1086–1094.

Li CY, Cox‐Foster D, Gray SM and Gildow F (2001) Vector specificity of Barley yellow dwarf virus (BYDV) transmission: identification of potential cellular receptors binding BYDV‐MAV in the aphid, Sitobion avenae. Virology 286: 125–133.

Liu S, Sivakumar S, Sparks WO, Miller WA and Bonning BC (2010) A peptide that binds the pea aphid gut impedes entry of Pea enation mosaic virus into the aphid hemocoel. Virology 401: 107–116.

Miller WA and Rasochova L (1997) Barley yellow dwarf viruses. Annual Review of Phytopathology 35: 167–190.

Ngumbi E, Eigenbrode SD, Bosque‐Pérez NA, Ding H and Rodriguez A (2007) Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV‐infected potato. Journal of Chemical Ecology 33: 1733–1747.

Pagán I and Holmes EC (2010) Long‐term evolution of the Luteoviridae: time scale and mode of virus speciation. Journal of Virology 84: 6177–6187.

Pazhouhandeh M, Dieterle M, Marrocco K et al. (2006) F‐box‐like domain in the polerovirus protein P0 is required for silencing suppressor function. Proceedings of the National Academy of Sciences of the USA 103: 1994–1999.

Peter KA, Liang D, Palukaitis P and Gray SM (2008) Small deletions in the Potato leafroll virus readthrough protein affect particle morphology, aphid transmission, virus movement and accumulation. Journal of General Virology 89: 2037–2045.

Peter KA, Gildow F, Palukaitis P and Gray SM (2009) The C terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. Journal of Virology 83: 5419–5429.

Revollon S, Strub JM, Fitchette AC et al. (2010) A reinvestigation provides no evidence for sugar residues on structural proteins of poleroviruses and argues against a role for glycosylation of virus structural proteins in aphid transmission. Virology 402: 303–314.

Rochow WF and Duffus JE (1981) Luteoviruses and yellows diseases. In: Kurstak E (ed.) Handbook of Plant Virus Infections and Comparative Diagnosis, pp. 147–170. Amsterdam, Netherlands: Elsevier/North‐Holland Biomedical Press.

Ryabov EV, Fraser G, Mayo MA, Barker H and Taliansky M (2001) Umbravirus gene expression helps Potato leafroll virus to invade mesophyll tissues and to be transmitted mechanically between plants. Virology 286: 363–372.

Savenkov EI and Valkonen JP (2001) Potyviral helper‐component proteinase expressed in transgenic plants enhances titers of Potato leaf roll virus but does not alleviate its phloem limitation. Virology 283: 285–293.

Seddas P, Boissinot S, Strub JM et al. (2004) Rack‐1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of Beet western yellows virus particles in the aphid. Virology 325: 399–412.

Smith HG and Barker H (eds) (1999) The Luteoviridae 297 pp. Oxon: CAB International.

Stevens M, Freeman B, Liu HY, Herrbach É and Lemaire O (2005) Beet poleroviruses: close friends or distant relatives? Molecular Plant Pathology 6: 1–9.

Terauchi H, Honda K, Yamagishi N et al. (2003) The N‐terminal region of the readthrough domain is closely related to aphid vector specificity of Soybean dwarf virus. Phytopathology 93: 1560–1564.

Thackray DJ, Diggle AJ and Jones RAC (2009) BYDV PREDICTOR: a simulation model to predict aphid arrival, epidemics of Barley yellow dwarf virus and yield losses in wheat crops in a Mediterranean‐type environment. Plant Pathology 58: 186–202.

Treder K, Kneller EL, Allen EM et al. (2008) The 3′ cap‐independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 14: 134–147.

Wang XF and Zhou GH (2003) Identification of a protein associated with circulative transmission of Barley yellow dwarf virus from cereal aphids, Schizaphis graminum and Sitobion avenae. Chinese Science Bulletin 48: 2083–2087.

Yang X, Thannhauser TW, Burrows M et al. (2008) Coupling genetics and proteomics to identify aphid proteins associated with vector‐specific transmission of polerovirus (Luteoviridae). Journal of Virology 82: 291–299.

Zhu YJ, McCafferty H, Osterman G et al. (2010) Genetic transformation with untranslatable coat protein gene of sugarcane yellow leaf virus reduces virus titers in sugarcane. Transgenic Research. doi: 10.1007/s11248‐010‐9432‐3.

Ziegler‐Graff V, Brault V, Mutterer JD et al. (1996) The coat protein of beet western yellows luteovirus is essential for systemic infection but the viral gene products P29 and P19 are dispensable for systemic infection and aphid transmission. Molecular Plant‐Microbe Interactions 9: 501–510.

Further Reading

Brault V, Ziegler‐Graff V and Richards KE (2001) Viral determinants involved in luteovirus–aphid interactions. In: Harris KE, Smith OP and Duffus JE (eds) Virus–Insect–Plant Interactions, pp. 207–232. San Diego: Academic Press.

Gray S and Gildow FE (2003) Luteovirus–aphid interactions. Annual Review of Phytopathology 41: 539–566.

Irwin ME and Thresh JM (1990) Epidemiology of barley yellow dwarf: a study in ecological complexity. Annual Review of Phytopathology 28: 393–424.

Mayo M and Ziegler‐Graff V (1996) Molecular biology of luteoviruses. Advances in Virus Research 46: 413–460.

Miller WA (1994) Luteoviruses. In: Webster RG and Granoff A (eds) Encyclopedia of Virology, pp. 792–798. London: Academic Press.

Miller WA, Liu S and Beckett R (2002) Barley yellow dwarf virus: Luteoviridae or Tombusviridae? Molecular Plant Pathology 3: 177–183.

Plumb RT (2002) Viruses of Poaceae: a case history in plant pathology. Plant Pathology 51: 673–826.

Taliansky M, Mayo MA and Barker H (2003) Potato leafroll virus: a classic pathogen shows some new tricks. Molecular Plant Pathology 4: 81–89.

Tamborindeguy C, Monsion B, Brault V et al. (2010) A genomic analysis of transcytosis in the pea aphid, Acyrthosiphon pisum, a mechanism involved in virus transmission. Insect Molecular Biology 19(suppl. 2): 259–272.

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Brault, Véronique, Herrbach, Etienne, and Rodriguez‐Medina, Caren(Mar 2011) Luteoviruses. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000751.pub3]