Localization, concentration, and transmission efficiency of banana bunchy top virus in four asexual lineages of Pentalonia aphids

Viruses

Volumn 5, Issue 2, 2013, Pages 758-776

  Watanabe, Shizu ^a   Greenwell, April M ^a,b   Bressan, Alberto ^a  

^a UNIVERSITY OF HAWAII   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Immunofluorescence localization; Pentalonia caladii; Pentalonia nigronervosa; Real time PCR

Indexed keywords

ALPINIA; ALPINIA PURPURATA; APHIDIDAE; ARTICLE; BABUVIRUS; COLOCASIA ESCULENTA; CONTROLLED STUDY; GENOTYPE; HELICONIACEAE; IMMUNOFLUORESCENCE; NONHUMAN; PENTALONIA CALADII; PENTALONIA NIGRONERVOSA; PLANT INSECT INTERACTION; PLANT LEAF; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SPECIES IDENTIFICATION; VIRUS TRANSMISSION;

ANIMALS; ANTIGENS, VIRAL; APHIDS; BABUVIRUS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HEMOLYMPH; INSECT VECTORS; MICROSATELLITE REPEATS; MULTILOCUS SEQUENCE TYPING; PLANT DISEASES; SALIVARY GLANDS;

EID: 84874438604     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v5020758     Document Type: Article

References (53)

1. Jones, D.R. Diseases of Banana, Abaca and Enset. CABI Publishing, UK, 2000, 544.
2. Dale, J.L.; Burns, T.; Oehlschlager, S.; Karan, M.; Harding, R. Banana bunchy top virus: Prospects for control through biotechnology. In Biotechnology Applications for Banana and Plantain Improvement, International Network for the Improvement of Banana and Plantain, San Jose, Costa Rica, 1992.
3. Kumar, P.L.; Hanna, R.; Alabi, O.J.; Soko, M.M.; Oben, T.T.; Vangu, G.H.P.; Naidu, R.A. Banana bunchy top virus in sub-Saharan Africa: Investigations on virus distribution and diversity. Virus Res. 2011, 159, 171-182.
4. Bhadra, P.; Agarwala, B.K. A comparison of fitness characters of two host plant-based congeneric species of the banana aphid, Pentalonia nigronervosa and P. caladii. J Insect Sci. 2010, 10.
5. Dale, J.L.; Harding, R.M. Banana bunchy top disease: current and future stratified for control. In Plant Virus Disease Control, Hadidi, A.; Khetarpal, R. K.; Kognanezawa, H. Eds.: APS Press, St. Paul, MN, USA, 1998; pp. 659-669.
6. Hooks, C.R.R.; Wright, M.G.; Kabasawa, D.S.; Manandhar, R.; Almeida, R.P.P. Effect of Banana bunchy top virus infection on morphology and growth characteristics of banana. Ann. Appl. Biol. 2008, 153, 1-9.
7. Vetten, H.J.; Chu, P.W.G.; Dale, J.L.; Harding, R.; Hu, J.; Katul, L.; Kojima, M.; Randles, J.W.; Sano, Y.; Thomas, J.E. Family Nanoviridae In Virus Taxonomy, Eighth report of the International Committee on Taxonomy of Viruses, Fauquet, C.M.; Mayo, M.A.; Maniloff, J.; Desselberger, U.; Ball, L.A. Eds.: Elsevier/Academic Press, London, United Kingdam, 2005; pp. 343-352.
8. Magee, C.J.P. Investigation on the bunchy top disease of the banana. In Council for Scientific and Industrial Research Bulletin No. 30, Government Printer, Melbourne, Australia, 1927; pp.86.
9. Hu, J.S.; Xu, M.Q.; Wu, Z.C.; Wang, M. Detection of Banana bunchy top virus in Hawaii. Plant Dis. 1993, 77, 952-952.
10. Anhalt, M.D.; Almeida, R.P.P. Effect of temperature, vector life stage, and plant access period on transmission of Banana bunchy top virus to Banana. Phytopathology 2008, 98, 743-748.
11. Bressan, A.; Watanabe, S. Immunofluorescence localisation of Banana bunchy top virus (family Nanoviridae) within the aphid vector, Pentalonia nigronervosa, suggests a virus tropism distinct from aphid-transmitted luteoviruses. Virus Res. 2011, 155, 520-525.
12. Watanabe, S.; Bressan, A. Tropism, compartmentalisation and retention of Banana bunchy top virus (Nanoviridae) in the aphid vector Pentalonia nigronervosa. J. Gen. Virol. 2013, 94, 209-219.
13. Brault, V.; Herrbach, E.; Reinbold, C. Electron microscopy studies on luteovirid transmission by aphids. Micron 2007, 38, 302-312.
14. Gray, S.; Gildow, F.E. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 2003, 41, 539-566.
15. Reinbold, C.; Herrbach, E.; Brault, V. Posterior midgut and hindgut are both sites of acquisition of cucurbit aphid-bome yellows virus in Myzus persicae and Aphis gossypii. J. Gen. Virol. 2003, 84, 3473-3484.
16. Gildow, F.E. Evidence for receptor-mediated endocytosis regulating luteovirus acquisition by aphids. Phytopathology 1993, 83, 270-277.
17. Reinbold, C.; Gildow, F.E.; Herrbach, E.; Ziegler-Graff, V.; Goncalves, M.C.; van den Heuvel, J.; Brault, V. Studies on the role of the minor capsid protein in transport of Beet western yellows virus through Myzus persicae. J. Gen. Virol. 2001, 82, 1995-2007.
18. Eastop, V.F. A taxonomic study of Australian Aphidoidea (Homoptera). Australian J. Zool. 1996, 14.
19. Blackman, R.L.; Eastop, V.F. Aphids on the world's crops: An identification and information guide, 2nd ed.; Chichester, John Wiley & Sons, Ltd., Chichester, England, 2000; pp. 466.
20. Venugopal, M.N. Viral diseases of cardamom (Elettaria cardamomum Maton) and their management. J. Spices Aromat. Crops 1995, 4, 32-39.
21. Foottit, R.G.; Maw, H.E.L.; Pike, K.S.; Miller, R.H. The identity of Pentalonia nigronervosa Coquerel and P. caladii van der Goot (Hemiptera: Aphididae) based on molecular and morphometric analysis. Zootaxa 2010, 25-38.
22. Galambao, M.B. The population genetics of Pentalonia nigronervosa and P. caladii (Hemiptera: Aphididae) in Hawaii. Master of Science, University of Hawaii, Honolulu, 2011; pp. 59.
23. Bourdin, D.; Rouze, J.; Tanguy, S.; Robert, Y. Variation among clones of Myzus persicae and Myzus nicotianae in the transmission of a poorly and a highly aphid-transmissible isolate of Potato leafroll luteovirus (PLRV). Plant Pathol. 1998, 47, 794-800.
24. Symmes, E.J.; Perring, T.M. Intraspecific variation in Zucchini yellow mosaic virus transmission by Myzus persicae and the impact of aphid host plant. J. Econ. Entomol. 2007, 100, 1764-1772.
25. Hu, J.S.; Wang, M.; Sether, D.; Xie, W.; Leonhardt, K.W. Use of polymerase chain reaction (PCR) to study transmission of Banana bunchy top virus by the banana aphid (Pentalonia nigronervosa). Ann. Appl. Biol. 1996, 128, 55-64.
26. Vetten, H.J.; Dale, J.L.; Grigoras, I.; Gronenborn, B.; Harding, R.; Randles, J.W.; Sano, Y.; Thomas, J.E.; Timchenko, T.; Yeh, H.-H. Family Nanoviridae. In Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses, King, A.M.Q.; Adams, M.J.; Carstens, E.C.; Lefkowitz, E.J. Eds.: Elsevier/Academic Press, London, United Kingdam, 2011; pp. 395-404.
27. Bencharki, B.; El Yamani, M.; Zaoui, D. Assessment of transmission ability of Barley yellow dwarf virus-PAV isolates by different populations of Rhopalosiphum padi and Sitobion avenae. Eur. J. Plant Pathol. 2000, 106, 455-464.
28. Dedryver, C.A.; Riault, G.; Tanguy, S.; Le Gallic, J.F.; Trottet, M.; Jacquot, E. Intra-specific variation and inheritance of BYDV-PAV transmission in the aphid Sitobion avenae. Eur. J. Plant Pathol. 2005, 111, 341-354.
29. Navas-Castillo, J.; Fiallo-Olive, E.; Sanchez-Campos, S. Emerging virus diseases transmitted by whiteflies. Ann. Rev. Phytopathol. 2011, 49, 219-248.
30. De Barro, P.J.; Liu, S.S.; Boykin, L.M.; Dinsdale, A.B. Bemisia tabaci: A statement of species status. Ann. Rev. Entomol. 2011, 56, 1-19.
31. Tamborindeguy, C.; Monsion, B.; Brault, V.; Hunnicutt, L.; Ju, H.J.; Nakabachi, A.; Van Fleet, E. A genomic analysis of transcytosis in the pea aphid, Acyrthosiphon pisum, a mechanism involved in virus transmission. Insect Mol. Biol. 2010, 19, 259-272.
32. Gildow, F.E.; Gray, S.M. The aphid salivary gland basal lamina as a selective barrier. associated with vector-specific transmission of Barley yellow dwarf luteoviruses. Phytopathology 1993, 83, 1293-1302.
33. Ghanim, M.; Medina, V. Localization of Tomato yellow leaf curl virus in its whitefly vector Bemisia tabaci. In Tomato yellow leaf curl virus disease, Management, molecular biology, breeding for resistance, Czosnek, H, Eds.; Springer, New York, USA, 2007; pp. 175-187.
34. Medina, V.; Pinner, M.S.; Bedford, I.D.; Achon, M.A.; Gemeno, C.; Markham, P.G. Immunolocalization of Tomato yellow leaf curl Sardinia virus in natural host plants and its vector Bemisia tabaci. J. Plant Pathol. 2006, 88, 299-308.
35. Hunter, W.B.; Hiebert, E.; Webb, S.E.; Tsai, J.H.; Polston, J.E. Location of geminiviruses in the whitefly Bemisia tabaci (Homoptera: Aleyrodidae). Plant Dis. 1998, 82, 1147-1151.
36. Lett, J.M.; Granier, M.; Hippolyte, I.; Grondin, M.; Royer, M.; Blanc, S.; Reynaud, B.; Peterschmitt, M. Spatial and temporal distribution of geminiviruses in leafhoppers of the genus Cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathology 2002, 92, 65-74.
37. Seddas, P.; Boissinot, S.; Strub, J.M.; Van Dorsselaer, A.; Van Regenmortel, M.H.V.; Pattus, F. Rack-1, GAPDH3, and actin: proteins of Myzus persicae potentially involved in the transcytosis of Beet western yellows virus particles in the aphid. Virology 2004, 325, 399-412.
38. Yang, X.L.; Thannhauser, T.W.; Burrows, M.; Cox-Foster, D.; Gildow, F.E.; Gray, S.M. Coupling genetics and proteomics to identify aphid proteins associated with vector-specific transmission of polerovirus (Luteoviridae). J. Virol. 2008, 82, 291-299.
39. Brault, V.; Tanguy, S.; Reinbold, C.; Le Trionnaire, G.; Arneodo, J.; Jaubert-Possamai, S.; Guernec, G.; Tagu, D. Transcriptomic analysis of intestinal genes following acquisition of Pea enation mosaic virus by the pea aphid Acyrthosiphon pisum. J. Gen. Virol. 2010, 91, 802-808.
40. Cilia, M.; Tamborindeguy, C.; Fish, T.; Howe, K.; Thannhauser, T.W.; Gray, S. Genetics coupled to quantitative intact proteomics links heritable aphid and endosymbiont protein expression to circulative polerovirus transmission. J. Virol. 2011, 85, 2148-2166.
41. Cilia, M.; Peter, K.A.; Bereman, M.S.; Howe, K.; Fish, T.; Smith, D.; Gildow, F.; MacCoss, M.J.; Thannhauser, T.W.; Gray, S. Discovery and targeted LC-MS/MS of purified polerovirus reveals differences in the virus-host interactome associated with altered aphid transmission. PLoS ONE 2012, 7(10): e48177. doi:10.1371/journal.pone.0048177.
42. Franz, A.W.E.; van der Wilk, F.; Verbeek, M.; Dullemans, A.M.; van den Heuvel, J. Faba bean necrotic yellows virus (genus Nanovirus) requires a helper factor for its aphid transmission. Virology 1999, 262, 210-219.
43. Tashiro, H. Selfwatering acrylic cages for confining insects and mites on detached leaves. J. Econ. Entomol. 1967, 60, 354-356.
44. Meirmans, P.G.; Van Tienderen, P.H. GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol. Ecol. Notes 2004, 4, 792-794.
45. Burns, T.M.; Harding, R.M.; Dale, J.L. The genome organization of Banana bunchy top virus: analysis of six ssDNA components. J. Gen. Virol. 1995, 76, 1471-1482.
46. Almeida, R.P.P.; Bennett, G.M.; Anhalt, M.D.; Tsai, C.W.; O'Grady, P. Spread of an introduced vector-borne banana virus in Hawaii. Mol. Ecol. 2009, 18, 136-146.
47. Xie, W.S.; Hu, J.S. Molecular cloning, sequence analysis, and detection of Bananana bunchy top virus in Hawaii Phytopathology 1995, 85, 339-347.
48. Hu, J.M.; Fu, H.C.; Lin, C.H.; Su, H.J.; Yeh, H.H. Reassortment and concerted evolution in Banana bunchy top virus genomes. J. Virol. 2007, 81, 1746-1761.
49. Wanitchakorn, R.; Hafner, G.J.; Harding, R.M.; Dale, J.L. Functional analysis of proteins encoded by Banana bunchy top virus DNA-4 to-6. J. Gen. Virol. 2000, 81, 299-306.
50. Mason, G.; Caciagli, P.; Accotto, G.P.; Noris, E. Real-time PCR for the quantitation of Tomato yellow leaf curl Sardinia virus in tomato plants and in Bemisia tabaci. J. Virol. Methods 2008, 147, 282-289.
51. Waterhouse, D.F. Pentalonia nigronervosa Coquerel. In Biological Control: Pacific Prospects, Waterhouse, E. F; Norris, K.R. Eds. Inkata Press, Melbourne, Australia, 1987; pp. 454.
52. Greenwell, A.M.; Bressan, A. Effect of species, genotype and host plant on the development, reproduction and survival of Pentalonia aphids on banana. Environ. Entomol. In review.
53. Jones, R.T.; Bressan, A.; Greenwell, A.M.; Fierer, N. Bacterial communities of two parthenogenetic aphid species co-colonizing two host plants across the Hawaiian Islands. Appl. Environ. Microbiol. 2011, 77: 8345-8349.