Plant Virus Transmission by Insects

Abstract

Most plant viruses depend on vectors for their survival and spread. Most vectors are piercing‐sucking insects that transmit plant viruses in either the circulative virus (CV) or noncirculative virus (NCV). NCV are carried on the lining cuticle of vectors stylets. CVs cross the vectors’ gut, move internally to the salivary glands (SG), cross the SG membranes to be ejected upon feeding.

Transmissibility of NCVs depends on motifs of coat protein and for Potyviruses and Caulimoviruses also on helper proteins (encoded by the virus). NCV proteins were found to associate with vectors’ cuticle proteins. Transmissibility of CVs depends on proteins comprising the virus capsid (the coat protein and the read‐through protein) and on symbionin (produced by vectors’ symbionts). Passage of CV through the gut has been also associated with vectors’ proteins.

To suppress plant virus epidemics, several control measures that interfere with vector landing or feeding are proposed.

Key concepts

  • Plants are rooted; therefore, plant viruses depend for their spread on insect vectors

  • Epidemics occur when a new virus or a new vector invade a new ecological niche.

  • Specificity between viruses and vector species may reflect the preference of the vector to the plant species.

  • Viruses that lost the ability to be transmitted by vectors serve to identify protein motifs that are associated with transmission.

  • Noncirculative viruses are transmitted by aphids during intracellular stylet penetrations whereas circulative viruses are transmitted during committed phloem ingestion.

  • Proteins encoded by the potyviruses and caulimoviruses are essential for assisting transmission by aphids.

  • Heteroencapsidation is responsible for expanding the vector range of luteoviruses.

  • Vector proteins were found to associate with viral proteins (for potyviruses, caulimoviruses and luteoviruses).

  • Insecticide are inefficient in preventing noncirculative plant viruses spread by vectors (the time needed to kill the vector is longer than the time needed to inoculate the host).

  • Control measures that affect vector landing or feeding are efficient in suppressing virus spread.

Keywords: transmission mechanisms; vector control; protein receptors

Figure 1.

Model describing the different strategies for virus–vector interaction in noncirculative transmission. These strategies enable retention of virus particles on the maxillary stylets at the surface of the cuticular lining. In the capsid strategy, a motif of the coat protein directly binds to the vector's receptor. In the helper strategy, virus–vector binding is mediated by the helper component (HC), which creates a ‘molecular bridge’ between the two. HC can be acquired alone and thereby allow HC‐transcomplementation as symbolized by the arrow and a different shading for the virus particle subsequently acquired. Reproduced by permission from Froissart, R, Michalakis, Y and Blanc, S (2002) Helper component transcomplementation in the vector transmission of plant viruses. Phytopathology92: 576–579.

Figure 2.

Schematic diagram of an aphid feeding and luteovirus transmission. Arrows indicate the circulative route for t PSG, principal salivary gland. From 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. Virology219: 57–65.

close

References

Blanc S, Hebrard E, Drucker M and Froissart R (2001) Caulimoviruses. In: Harris KF, Smith OP and Duffus JE (eds) Virus‐Insect‐Plant Interactions, pp. 143–166. New York: Academic Press.

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

Dombrovsky A, Gollop N, Chen S, Chejanovsky N and Raccah B (2007) In vitro association between the helper component‐proteinase of Zucchini yellow mosaic virus and cuticle proteins of Myzus persicae. Journal of General Virology 88: 1602–1610.

Drucker M, Froissart R, Hebrard E et al. (2002) Intracellular distribution of viral gene products regulates a complex mechanism of cauliflower mosaic virus acquisition by its aphid vector. Proceedings of the National Academy of Sciences of the USA 99: 2422–2427.

Fereres A and Collar JE (2001) In: Harris KF, Smith OP and Duffus JE (eds) Virus‐Insect‐Plant Interactions: Analysis of Noncirculative Transmission by Electrical Penetration Graphs, pp. 87–109. New York: Academic Press.

Gergerich RC (2001) Mechanism of virus transmission by leaf‐feeding beetles. In: Harris KF, Smith OP and Duffus JE (eds) Virus‐Insect‐Plant Interactions, pp. 133–142. New York: Academic Press.

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

Hull R (1994) Molecular biology of plant‐virus‐vector interactions. Advances in Disease Vector Research 10: 361–386.

Moreno A, Palacios L, Blanc S and Fereres A (2005) Intracellular salivation is the mechanism involved in the inoculation of cauliflower mosaic virus by its major vectors Brevicoryne brassicae and Myzus persicae. Annals of the Entomological Society of America 98: 763–769.

Perry KL (2001) Cucumoviruses. In: Harris KF, Smith OP and Duffus JE (eds) Virus‐Insect‐Plant Interactions, pp. 167–180. New York: Academic Press.

Pirone TP and Perry KL (2002) Aphids: non‐persistent transmission. Advances in Botanical Research 36: 1–19.

Raccah B (1986) Nonpersistent viruses: epidemiology and control. Advances in Virus Research 31: 387–429.

Raccah B, Huet H and Blanc S (2001) Potyviruses. In: Harris KF, Smith OP and Duffus JE (eds) Virus‐Insect‐Plant Interactions, pp. 181–206. New York: Academic Press.

Raccah B, Roistacher C and Barabagallo S (1990) Transmission of semipersistent viruses with special emphasis on Citrus tristeza virus. Advances in Disease Vector Research 6: 301–340.

Raviv M and Antignus Y (2004) UV radiation effects on pathogens and insect pests of greenhouse‐grown crops. Photochemistry and Photobiology 79: 219–226.

Uzest M, Gargani D, Drucker M et al. (2007) A protein key to plant virus transmission at the tip of the insect vector stylet. Proceedings of the National Academy of Sciences of the USA 104: 17959–17964.

Yang X, Thannhauser TW, Burrows MM 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.

Further Reading

Ammar ED (1994) Propagative transmission of plant and animal viruses by insects: factors affecting vector specificity and competence. Advances in Virus Vector Research 10: 289–331.

Belliure B, Janssen A, Maris PC, Peters D and Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters 8: 70–79.

Dombrovsky A, Huet H, Chejanovsky N and Raccah B (2005) Aphid transmission of a potyvirus depends on suitability of the helper component and the N terminus of the coat protein. Archives of Virology 150: 287–298.

Irwin ME, Kampmeier GE and Weisser WW (2007) Aphid Movement: Process and Consequences. In: van Emden HF and Harrington R (eds) Aphids as Crop Pests, pp. 153–186. Wallingford: CABI Publishing.

Kumar P and Poehling HM (2006) UV‐blocking plastic films and nets influence vectors and virus transmission on greenhouse tomatoes in the humid tropics. Environmental Entomology 35: 1069–1082.

Ng JCK and Falk BW (2006) Virus‐vector interactions mediating nonpersistent and semipersistent transmission of plant viruses. Annual Review of Phytopathology 44: 183–212.

Ng JCK and Perry KL (2004) Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5: 505–511.

Perring TM, Gruenhagen NM and Farrar CA (1999) Management of plant viral diseases through chemical control of insect vectors. Annual Review of Entomology 44: 457–481.

Pirone TP and Blanc S (1996) Helper‐dependent vector transmission of plant viruses. Annual Review of Phytopathology 34: 227–247.

Ruiz‐Ferrer V, Boskovic J, Alfonso C et al. (2005) Structural analysis of tobacco etch potyvirus HC‐Pro oligomers involved in aphid transmission. Journal of Virology 79: 3758–3765.

Seddas P and Boissinot S (2006) Glycosylation of beet western yellows virus proteins is implicated in the aphid transmission of the virus. Archives of Virology 151: 967–984.

Syller J (2005) The roles and mechanisms of helper component proteins encoded by potyviruses and caulimoviruses. Physiological and Molecular Plant Pathology 67: 119–130.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Raccah, B, and Fereres, A(Mar 2009) Plant Virus Transmission by Insects. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000760.pub2]