Luteovirids

Abstract

Members of the Luteoviridae family, or luteovirids, are plant viruses that can infect a wide range of host plants, including many important crops such as cereals, potato, sugar beet, cucurbits, legumes and sugarcane. Their icosahedral virions contain a single positive‐sense 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.

More data are accumulating on plant–luteovirid relationships and in particular on the mechanism developed by the virus to overcome plant defence. The tight interaction between luteovirids, their aphid vector and their host plant are also extensively studied. Information from these studies together with a better understanding of the epidemiology of luteovirids will help to combat their detrimental effects on crops.

Key Concepts

  • Luteovirids 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.
  • Luteovirids are confined to phloem tissue, but the causes of their phloem restriction are not completely deciphered.
  • Luteovirids circulate in the vector aphid's body, without any replication, by crossing the gut and the accessory salivary gland epithelia.
  • Epidemiology of luteovirids 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; gene expression; aphid transmission; epidemiology; virus control

Figure 1. Genome organisation and map of the translation products of the type‐members of each genus: (a) Barley yellow dwarf virus‐PAV, (b) Potato leafroll virus and (c) Pea enation mosaic virus‐1. Purple rectangles are open readings frames (ORFs). Blue, orange and green rectangles are proteins translated from ORFs and their molecular weight in kilo Dalton (K). VPg: Viral protein genome‐linked, RNAsg: Subgenomic RNA.
Figure 2. Purified viral particles of turnip yellows virus. Courtesy of C. Reinbold. Bar, 100 nm.
Figure 3. Diagram of the route of luteovirid virions through the aphid vector. AG, accessory salivary gland; PG, principal salivary gland. Source: Adapted from Smith HG and Barker H (eds) (1999) The Luteoviridae, 297 pp. Oxon: CAB International.
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References

Alexander MM, Mohr JP, DeBlasio SL, et al. (2017) Insights in luteovirid structural biology guided by chemical cross‐linking and high resolution mass spectrometry. Virus Research 241: 42–52.

Almasi MA, Manesh ME, Jafary H, et al. (2013) Visual detection of Potato leafroll virus by loop‐mediated isothermal amplification of DNA with the GeneFinder™ dye. Journal of Virology Methods 192: 51–54.

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.

Bastet A, Lederer B, Giovinazzo N, et al. (2018) Trans‐species synthetic gene design allows resistance pyramiding and broad‐spectrum engineering of virus resistance in plants. Plant Biotechnology Journal 16: 1569–1581.

Baumberger N, Tsai CH, Lie M, et al. (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.

Blanc S and Michalakis Y (2016) Manipulation of hosts and vectors by plant viruses and impact of the environment. Current Opinion in Insect Science 16: 36–43.

Boissinot S, Erdinger M, Monsion B, et al. (2014) Both structural and non‐structural forms of the readthrough protein of Cucurbit aphid‐borne yellows virus are essential for efficient systemic infection of plants. PLoS One 9: e93448.

Boukari W, Kaye C, Wei CY, et al. (2019) Field infection of virus‐free sugarcane by sugarcane yellow leaf virus and effect of yellow leafon sugarcane grown on organic and on mineral soils in Florida. Plant Disease 103: 2367–2373.

Bouvaine S, Boonham N and Douglas AE (2011) Interactions between a Luteovirus and the GroEL chaperonin protein of the symbiotic bacterium Buchnera aphidicola of aphids. Journal of General Virology 92: 1467–1474.

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

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.

Byrne MJ, Steele JFC, Hesketh EL, et al. (2019) Combining transient expression and cryo‐EM to obtain high‐resolution structures of luteovirid particles. Structure 27: 1761–1770.

Carmo‐Sousa A, Moreno MP, Plaza M, et al. (2016) Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Annals of Applied Biology 169: 284–297.

Chavez CR, Cilia M, Weisbrod CR, et al. (2012) Cross‐linking measurements of the Potato leafroll virus reveal protein interaction topologies required for virion stability, aphid transmission, and virus‐plant interactions. Journal of Proteome Research 11: 2968–2981.

Chay CA, Gunasinge UB, Dinesh‐Kumar SP, et al. (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, Winder L, Armstrong KF, et al. (2011) Detection and discrimination of members of the family Luteoviridae by real‐time PCR and SYBR® GreenER™ melting curve analysis. Journal of Virology Methods 171: 46–52.

Choudhury S, Hu H, Meinke H, et al. (2017) Barley yellow dwarf viruses: infection mechanisms and breeding strategies. Euphytica 213: 168.

Cilia M, Tamborindeguy C, Fish T, et al. (2010) Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. Journal of Virology 85: 2148–2166.

Cilia M, Peter KA, Bereman MS, et al. (2012) Discovery and targeted LC‐MS/MS of purified polerovirus reveals differences in the virus‐host interactome associated with altered aphid transmission. PLoS One 7: e48177.

Cilia M, Johnson R, Sweeney M, et al. (2014) Evidence for lysine acetylation in the coat protein of a polerovirus. Journal of General Virology 95: 2321–2327.

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

DeBlasio SL, Chavez JD, Alexander MM, et al. (2016) Visualization of host‐polerovirus interaction topologies using protein interaction reporter technology. Journal of Virology 90 (4): 1973–1987.

DeBlasio SL, Xu Y, Johnson RS, et al. (2018a) The Interaction dynamics of two Potato leafroll virus movement proteins affects their localization to the outer membranes of mitochondria and plastids. Viruses 10: 585.

DeBlasio SL, Rebelo AR, Parks K, et al. (2018b) Disruption of chloroplast function through downregulation of phytoene desaturase enhances the systemic accumulation of an aphid‐borne, phloem‐restricted virus. Molecular Plant‐Microbe Interactions 31: 1095–1110.

Derrien B, Baumberger N, Schepetilnikov M, et al. (2012) Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proceedings of the National Academy of Sciences of the USA 109: 15942–15946.

Fereres A and Moreno A (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research 141: 158–168.

Fusaro AF, Correa RL, Nakasugi K, et al. (2012) The Enamovirus P0 protein is a silencing suppressor which inhibits local and systemic RNA silencing through AGO1 degradation. Virology 426: 178–187.

Fusaro AF, Barton DA, Nakasugi K, et al. (2017) The Luteovirus P4 movement protein is a suppressor of systemic RNA silencing. Viruses 9: 294.

Ghosh S, Kanakala S, Lebedev G, et al. (2019) Transmission of a new polerovirus infecting pepper by the whitefly Bemisia tabaci. Journal of Virology 93: e00488–e00419.

Hackenberg H, Asare‐Bediako BA, et al. (2020) Identification and QTL mapping of resistance to Turnip yellows virus (TuYV) in oilseed rape, Brassica napus. Theoretical and Applied Genetics 133: 383–393.

Heck M and Brault V (2018) Targeted disruption of aphid transmission: a vision for the management of crop diseases caused by Luteoviridae members. Current Opinion in Virology 33: 24–32.

Hipper C, Monsion B, Bortolamiol‐Bécet D, et al. (2014) Formation of virions is strictly required for Turnip yellows virus long‐distance movement in plants. Journal of General Virology 95: 496–505.

Hwang YT, Kalischuk M, Fusaro AF, et al. (2013) Small RNA Sequencing of Potato leafroll virus‐infected plants reveals an additional subgenomic RNA encoding a sequence‐specific RNA‐binding protein. Virology 438: 61–69.

ICTV (2018) Virus Taxonomy: 2018b Release. Available at: https://talk.ictvonline.org/taxonomy/ (Retrieved on April 2020).

Ingwell LL, Eigenbrode SD and Bosque‐Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Science Reports 2: 578.

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.

Jarošová J, Beoni E and Kundu JK (2016) Barley yellow dwarf virus resistance in cereals: approaches, strategies and prospects. Field Crops Research 198: 200–214.

Ju J, Kim K, Lee KJ, et al. (2017) Localization of Barley yellow dwarf virus movement protein modulating programmed cell death in Nicotiana benthamiana. Plant Pathology Journal 33: 53–65.

Kajiwara H and Murakami R (2017) Application of RT‐PCR and MALDI‐TOF MS for the detection of RNA luteovirus. Analytical Biochemistry 539: 45–47.

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, et al. (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.

Linz LB, Liu S, Chougule NP, et al. (2015) In vitro evidence supports membrane alanyl aminopeptidase N as a receptor for a plant virus in the pea aphid vector. Journal of Virology 89: 11203–11212.

Mauck KE, Chesnais Q and Shapiro LR (2018) Evolutionary determinants of host and vector manipulation by plant viruses. Advances in Virus Research 101: 189–250.

Mauck KE, Kenney J and Chesnais Q (2019) Progress and challenges in identifying molecular mechanisms underlying host and vector manipulation by plant viruses. Current Opinion in Insect Science 33: 7–18.

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

Miller WA, Jackson J and Feng Y (2015) Cis‐ and trans‐regulation of luteovirus gene expression by the 3' end of the viral genome. Virus Research 3: 37–45.

Mostert I, Visser M, Gazendam I, et al. (2020) Complete genome sequence of a novel polerovirus in Ornithogalum thyrsoides from South Africa. Archives of Virology 165: 483–486.

Mulot M, Monsion B, Boissinot S, et al. (2018) Transmission of Turnip yellows virus by Myzus persicae is reduced by feeding aphids on double‐stranded RNA targeting the ephrin receptor protein. Frontiers in Microbiology 9: 457.

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, et al. (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, et al. (2009) The C terminus of the polerovirus p5 readthrough domain limits virus infection to the phloem. Journal of Virology 83: 5419–5429.

Pinheiro PV, Ghanim M, Alexander M, et al. (2017) Host plants indirectly influence plant virus transmission by altering gut cysteine protease activity of aphid vectors. Molecular & Cellular Proteomics 16: S230–S243.

Reinbold C, Lacombe S, Ziegler‐Graff V, et al. (2013) Closely related poleroviruses depend on distinct translation initiation factors to infect Arabidopsis thaliana. Molecular Plant‐Microbe Interactions 26: 257–265.

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.

Rodriguez‐Medina C, Boissinot S, Chapuis S, et al. (2015) A protein kinase binds the C‐terminal domain of the readthrough protein of Turnip yellows virus and regulates virus accumulation. Virology 486: 44–53.

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

Schmitz J, Stussi‐Garaud C, Tacke E, et al. (1997) In situ localization of the putative movement protein (pr17) from Potato leafroll luteovirus (PLRV) in infected and transgenic potato plants. Virology 235: 311–322.

Schoeny A, Desbiez C, Millot P, et al. (2017) Impact of Vat resistance in melon on viral epidemics and genetic structure of virus populations. Virus Research 241: 105–115.

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.

Shaw AK, Igoe M, Power AG, et al. (2019) Modeling approach influences dynamics of a vector‐borne pathogen system. Bulletin of Mathematical Biology 81: 2011–2028.

Shepardson S, Esau K and McCrum R (1980) Ultrastructure of potato leaf phloem infected with potato leafroll virus. Virology 105: 379–392.

Smirnova E, Firth AE, Miller WA, et al. (2015) Discovery of a small non‐AUG‐initiated ORF in Poleroviruses and Luteoviruses that is required for long‐distance movement. PLoS Pathogens 11: e1004868.

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

Sokolova M, Prüfer D, Tacke E, et al. (1997) The Potato leafroll virus 17K movement protein is phosphorylated by a membrane‐associated protein kinase from potato with biochemical features of protein kinase C. FEBS Letters 400: 201–205.

Stevens M, Freeman B, Liu HY, et al. (2005) Beet poleroviruses: close friends or distant relatives? Molecular Plant Pathology 6: 1–9.

Sun Q, Li YY, Wang Y, Zhao HH, et al. (2018) Brassica yellows virus P0 protein impairs the antiviral activity of NbRAF2 in Nicotiana benthamiana. Journal of Experimental Botany 69: 3127–3139.

Tacke E, Schmitz J, Prüfer D, et al. (1993) Mutational analysis of the nucleic acid‐binding 17 kDa phosphoprotein of potato leafroll luteovirus identifies an amphipathic alpha‐helix as the domain for protein/protein interactions. Virology 97: 274–282.

Tamborindeguy C, Bereman MS, DeBlasio S, et al. (2013) Genomic and proteomic analysis of Schizaphis graminum reveals cyclophilin proteins are involved in the transmission of cereal yellow dwarf virus. PLoS One 8: e71620.

Terradot L, Souchet M, Tran V, et al. (2001) Analysis of a three‐dimensional structure of Potato leafroll virus coat protein obtained by homology modeling. Virology 286: 72–82.

Van den Eyden R, Van Leeuwen T and Haesaert G (2020) Identifying drivers of spatio‐temporal dynamics in barley yellow dwarf virus epidemiology as a critical factor in disease control. Pest Management Science 76: 2548–2556. DOI: 10.1002/ps.5851.

Villamor DEV, Mekuria TA, Pillai SS, et al. (2016) High‐throughput sequencing identifies novel viruses in nectarine: insights to the etiology of stem‐pitting disease. Virology 106: 519–527.

Walls J, Rajotte E and Rosa C (2019) The past, present, and future of Barley yellow dwarf management. Agriculture 9: 23.

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.

Wang H, Wu K, Liu Y, et al. (2015a) Integrative proteomics to understand the transmission mechanism of Barley yellow dwarf virus‐GPV by its insect vector Rhopalosiphum padi. Scientific Reports 5: 10971.

Wang KD, Empleo R, Nguyen TTV, et al. (2015b) Elicitation of hypersensitive responses in Nicotiana glutinosa by the suppressor of RNA silencing Protein P0 from poleroviruses. Molecular Plant Pathology 16: 435–448.

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.

Yvon M, Vile D, Brault V, et al. (2017) Drought reduces transmission of Turnip yellows virus, an insect‐vectored circulative virus. Virus Research 241: 131–136.

Zhao P, Liu Q, Miller WA, et al. (2017) Eukaryotic translation Initiation Factor 4G (eIF4G) coordinates interactions with eIF4A, eIF4B, and eIF4E in binding and translation of the Barley yellow dwarf virus 3' Cap‐Independent Translation Element (BTE). The Journal of Biological Chemistry 292: 5921–5931.

Zhu YJ, McCafferty H, Osterman G, et al. (2011) Genetic transformation with untranslatable coat protein gene of Sugarcane yellow leaf virus reduces virus titers in sugarcane. Transgenic Research 20: 503–512.

Zhuo T, Li YY, Xiang HY, et al. (2014) Amino acid sequence motifs essential for P0‐mediated suppression of RNA silencing in an isolate of Potato Leafroll Virus from inner Mongolia. Molecular Plant‐Microbe Interactions 27: 515–527.

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.

Ziegler‐Graff V (2020) Molecular insights into host and vector manipulation by plant viruses. Viruses 12: 263.

Further Reading

Bosque‐Pérez NA and Eigenbrode SD (2011) The influence of virus‐induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Research 159: 201–205.

Eigenbrode SD, Bosque‐Pérez NA and Davis TS (2018) Insect‐borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annual Review of Entomology 63: 169–191.

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

Mauck KE, Bosque‐Pérez NA, Eigenbrode SD, et al. (2012) Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Functional Ecology 26: 1162–1175.

Mauck KE (2016) Variation in virus effects on host plant phenotypes and insect vector behavior: what can it teach us about virus evolution? Current Opinion in Virology 21: 114–123.

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

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

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

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Boissinot, Sylvaine, Brault, Véronique, and Herrbach, Etienne(Sep 2020) Luteovirids. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029206]