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REVIEW ARTICLE

Baculovirus-based strategies for the management of insect pests: a focus on development and application in South Africa

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Pages 1-20 | Received 08 Mar 2014, Accepted 24 Jul 2014, Published online: 07 Oct 2014

References

  • Abdulkadir, F., Marsberg, T., Knox, C. M., Hill, M. P., & Moore, S. D. (2013). Morphological and genetic characterisation of a South African Plutella xylostella granulovirus isolate. African Entomology, 21, 168–171. doi:10.4001/003.021.0101
  • Agathos, S. N. (1991). Mass production of viral insecticides. In K. Maramorosch (Ed.), Biotechnology for biological control of pests and vectors (pp. 217–235). Boca Raton, FL: CRC Press.
  • Angelini, A., Amargier, A., Vandamme, P., & Duthoit, J. L. (1965). Une virose á granules chez le lepidoptére Argyroploce leucotreta [The granulosis-virus disease of the lepidopteran Argyroploce leucotreta]. Coton Fibres Tropicales, 20, 277–282.
  • Arthurs, S. P., & Lacey, L. A. (2004). Field evaluation of commercial formulations of the codling moth granulovirus: persistence of activity and success of seasonal applications against natural infestations of codling moth in Pacific Northwest apple orchards. Biological Control, 31, 388–397. doi:10.1016/j.biocontrol.2004.05.004
  • Arthurs, S. P., Lacey, L. A., & Behle, R. W. (2006). Evaluation of spray-dried lignin-based formulations and adjuvants as ultraviolet light protectants for the granulovirus of the codling moth, Cydia pomonella (L). Journal of Invertebrate Pathology, 93, 88–95. doi:10.1016/j.jip.2006.04.008
  • Asayama, T., & Osaki, N. (1970). A granulosis of the diamondback moth, Plutella xylostella. Journal of Invertebrate Pathology, 15, 284–286. doi:10.1016/0022-2011(70)90248-X
  • Bale, J. S., van Lenteren, J. C., & Bigler, F. (2008). Biological control and sustainable food production. Philosophical Transactions of the Royal Society, 363, 761–776. doi:10.1146/annurev.en.31.010186.001005
  • Ballard, J., Ellis, D. J., & Payne, C. C. (2000). The role of formulation additives in increasing the potency of Cydia pomonella granulovirus for codling moth larvae, in laboratory and field experiments. Biocontrol Science and Technology, 10, 627–640. doi:10.1080/095831500750016424
  • Barnes, M. M. (1991). Codling moth occurrence, host race formation and damage. In L. P. S. van der Geest & H. H. Evenhuis (Eds.), Tortricid pests: Their biology, natural enemies and control (pp. 313–327). Amsterdam: Elsevier.
  • Bell, J. C., & McGeoch, M. A. (1996). An evaluation of the pest status and research conducted on phytophagous Lepidoptera on cultivated plants in South Africa. African Entomology, 4, 161–170.
  • Berling, M., Blachere-Lopez, C., Soubabere, O., Lery, X., Bonhomme, A., Sauphanor, B., & Lopez-Ferber, M. (2009). Cydia pomonella granulovirus genotypes overcome virus resistance in codling moth and improve virus efficacy by selection against resistant hosts. Applied and Environmental Microbiology, 75, 925–930. doi:10.1128/AEM.01998-08
  • Besse, S., Crabos, L., Soubabere, O., Bonhomme, A., Lopez-Ferber, M., Berling, M., Sauphanor, B., & Ondet, S. (2011). The new CpGV-R5 variants overcome the codling moth resistance to the virus. IOBC/wprs Bulletin, 66, 397–400.
  • Black, B. C., Brennan, L. A., Dierks, P. M., & Gard, I. E. (1997). Commercialization of baculoviral insecticides. In L. K. Miller (Ed.), The baculoviruses (pp. 341–387). New York, NY: Plenum Press.
  • Blissard, G. W., & Rohrmann, G. F. (1990). Baculovirus diversity and molecular biology. Annual Review of Entomology, 35, 127–155. doi:10.1146/annurev.en.35.010190.001015
  • Bonning, B. C., & Hammock, B. D. (1996). Development of recombinant baculoviruses for insect control. Annual Review of Entomology, 41, 191–210. doi:10.1146/annurev.en.41.010196.001203
  • Briese, D. T. (1981). The incidence of parasitism and disease in field populations of the potato moth Phthorimaea operculella (Zeller) in Australia. Journal of the Australian Entomological Society, 20, 319–326. doi:10.1111/j.1440-6055.1981.tb01057.x
  • Broodryk, S. W., & Pretorius, L. M. (1974). Occurrence in South Africa of a granulosis virus attacking potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Journal of the Entomological Society of South Africa, 37, 125–128.
  • Bullock, H. R., Hollingsworth, J. R., & Harstack, A. W. (1970). Virulence of Heliothis nuclear polyhedrosis virus exposed to monochromatic ultraviolet irradiation. Journal of Invertebrate Pathology, 16, 419–422. doi:10.1016/0022-2011(70)90161-8
  • Burges, H. D., & Jones, K. A. (1998). Formulation of bacteria, viruses and protozoa to control insects. In H. D. Burges (Ed.), Formulation of microbial biopesticides: Beneficial microorganisms, nematodes and seed treatments (pp. 33–127). Dordrecht: Kluwer Academic Publishers.
  • Carpio, C., Dangles, O., Dupas, S., Léry, X., López-Ferber, M., Orbe, K., & Zeddam, J.-L. (2013). Development of a viral biopesticide for the control of the Guatemala potato tuber moth Tecia solanivora. Journal of Invertebrate Pathology, 112, 184–191. doi:10.1016/j.jip.2012.11.014
  • Chandler, D., Bailey, A. S., Tatchell, M., Davidson, G., Greaves, J., & Grant, W. P. (2011). The development, regulation and use of biopesticides for integrated pest management. Philosophical Transactions of the Royal Society, 366, 1987–1998. doi:10.1016/j.tree.2006.02.007
  • Cherry, A. J., Mercardier, G., Meikle, W., Castelo-Branco, M., & Schroer, S. (2004). The role of entomopathogens in DBM control. In D. Bordat & A. A. Kirk (Eds.), Improving Biocontrol of Plutella xylostella (pp. 51–70). CIRAD, ISBN 2 87614 5707. Proceedings of the International Symposium in Montpellier, France, 21–24 Oct 2002.
  • Claus, J. D., Gioria, V. V., Micheloud, G. A., & Visnovsky, G. (2012). Production of insecticidal baculoviruses in insect cell cultures: Potential and limitations. In S. Soloneski & M. Larramendy (Eds.), Insecticides – basic and other applications (pp. 127–152). Rijeka: INTECH. Retrieved from http://dx.doi.org/10.5772/29551
  • Copping, L. G., & Menn, J. J. (2000). Biopesticides: A review of their action, applications and efficacy. Pest Management Science, 56, 651–676. doi:10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U
  • Cory, J. S., & Myers, J. H. (2003). The ecology and evolution of insect baculoviruses. Annual Review of Ecology, Evolution and Sytematics, 34, 239–272. doi:10.1146/annurev.ecolsys.34.011802.132402
  • Crook, N. E., Spencer, R. A., Payne, C. C., & Leisy, D. J. (1985). Variation in Cydia pomonella granulosis virus isolates and physical maps of the DNA from three variants. Journal of General Virology, 66, 2423–2430. doi:10.1099/0022-1317-66-11-2423
  • Davis, M. A., Chew, M. K., Hobbs, R. J., Lugo, A. E., Ewel, J. J., Vermeij, G. J., & Briggs, J. C. (2011). Don't judge species on their origins. Nature, 474, 153–154. doi:10.1038/474153a
  • Dunley, J. E., & Welter, S. C. (2000). Correlated insecticide cross-resistance in azinphosmethyl resistant codling moth (Lepidoptera: Tortricidae). Journal Economic Entomology, 93, 955–962. doi:10.1603/0022-0493-93.3.955
  • Eberle, K. E., Asser-Kaiser, S., Sayed, S. M., Nguyen, H. T., & Jehle, J. A. (2008). Overcoming the resistance of codling moth against conventional Cydia pomonella granulovirus (CpGV-M) by a new isolate CpGV-I12. Journal of Invertebrate Pathology, 98, 293–298. doi:10.1016/j.jip.2008.03.003
  • Eberle, K. E., Sayed, S., Rezapanah, M., Shojai-Estabragh, S., & Jehle, J. A. (2009). Diversity and evolution of the Cydia pomonella granulovirus. Journal of General Virology, 90, 662–671. doi:10.1099/vir.0.006999-0
  • Eldridge, R., Horodyski, F. M., Morton, D. B., O'Reilly, D., Truman, J. W., & Riddiford, L. M. (1991). Expression of an eclosion hormone gene in insect cells using baculovirus vectors. Insect Biochemistry, 21, 341–351. doi:10.1016/0020-1790(91)90025-A
  • El-Sayed, A., El-Sheikh, E. A., Kamita, S. G., Vu, K., & Hammock, B. D. (2011). Improved insecticidal efficacy of a recombinant baculovirus expressing mutated JH esterase from Manduca sexta. Biological Control, 58, 354–361. doi:10.1016/j.biocontrol.2011.06.002
  • Engelhard, E. K., Kammorgan, L. N. W., Washburn, J. O., & Volkman, L. E. (1994). The insect tracheal system: A conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proceedings of the National Academy of Sciences USA, 91, 3224–3227. doi:10.1073/pnas.91.8.3224
  • Erlandson, M. (2008). Insect pest control by viruses. In B. W. J. Mahy & M. H. V. Van Regenmortel (Eds.), Encyclopedia of virology, Vol. 3 (3rd ed., pp. 125–133). Oxford: Elsevier.
  • Federici, B. A., Bigot, Y., Granados, R. R., Hamm, J. J., Miller, L. K., Newton, I., & Vlak, J. M. (2005). Family Ascoviridae. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, & L. A. Ball (Eds.), Virus taxonomy. Eighth report of the international committee on taxonomy of viruses (pp. 269–274). San Diego, CA: Elsevier Academic Press.
  • Fitt, G. P. (1989). The ecology of Heliothis species in relation to agroecosystems. Annual Review of Entomology, 34, 17–53. doi:10.1146/annurev.en.34.010189.000313
  • Fritsch, E. (1989). Das Granulosevirus des Falschen Apfelwicklers, Cryptophlebia leucotreta (Meyrick) [The granulovirus of the false codling moth, Cryptophlebia leucotreta] ( Dissertation), Fachbereich Biologie der TU Darmstadt, Darmstadt, Germany.
  • Fritsch, E., Huber, J., & Backhaus, H. (1990, August 20–24). CpGV as a tool in the risk assessment of genetically engineered baculoviruses. Proceedings and abstracts of the Vth international colloquium on invertebrate pathology and microbial control, Adelaide, Australia. pp. 439–443.
  • Fritsch, E., Undorf-Spahn, K., Kienzle, J., Zebitz, C. P. W., & Huber, J. (2005). Codling moth granulovirus: First indication of variations in the susceptibility of local codling moth populations. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 57, 29–34.
  • Fritsch, E., Undorf-Spahn, K., Kienzle, J., Zebitz, C. P. W., & Huber, J. (2006, January–February). Codling moth granulovirus: Variations in the susceptibility of local codling moth populations. Ecofruit – Proceedings to the 12th International Conference on Cultivation. Technique and Phytopathological Problems in Organic Fruit-Growing. Föko e. V, Weinsberg, Germany. pp. 7–13.
  • Fuentes-Contreras, E., Reyes, M., Barros, W., & Sauphanor, B. (2007). Evaluation of azinphos-methyl resistance and activity of detoxifying enzymes in codling moth (Lepidoptera: Tortricidae) from central chile. Journal of Economic Entomology, 100, 551–556. doi:10.1603/0022-0493(2007)100[551:EOARAA]2.0.CO;2
  • Furlong, M. J., Wright, D. J., & Dosdall, L. M. (2013). Diamondback moth ecology and management: Problems, progress, and prospects. Annual Reviews in Entomology, 58, 517–541. doi:10.1146/annurev-ento-120811-153605
  • Fuxa, J. R. (2004). Ecology of insect nucleopolyhedroviruses. Agriculture Ecosystems and Environment, 103(1), 27–43. doi:10.1016/j.agee.2003.10.013
  • Goodman, C. L., & McIntosh, A. H. (1994). Production of baculoviruses for insect control using cell culture. In K. Maramorosch & A. H. McIntosh (Eds.), Insect cell biotechnology (pp. 33–56). Boca Raton, FL: CRC Press.
  • Goodman, C. L., McIntosh, A. H., El Sayed, G. N., Grasela, J. J., & Stiles, B. (2001). Production of selected baculoviruses in newly established lepidopteran cell lines. In Vitro Cellular Developmental BiologyAnimal, 37, 374–379. doi:10.1007/BF02577574
  • Grzywacz, D., Rossbach, A., Rauf, A., Russell, D. A., Srinivasan, R., & Shelton, A. M. (2010). Current control methods for diamondback moth and other brassica insect pests and the prospects for improved management with lepidopteran-resistant Bt vegetable brassicas in Asia and Africa. Crop Protection, 29, 68–79. doi:10.1016/j.cropro.2009.08.009
  • Hajek, A. (2004). Natral enemies: An introduction to biological control. Cambridge: Cambridge University Press.
  • Harvey, J. P., & Volkman, L. E. (1983). Biochemical and biological variation of Cydia pomonella (codling moth) granulosis virus. Virology, 124, 21–34. doi:10.1016/0042-6822(83)90287-8
  • Hashimoto, Y., Hayakawa, T., Ueno, Y., Fujita, T., Sano, Y., & Matsumoto, T. (2000). Sequence analysis of the Plutella xylostella granulovirus genome. Virology, 275, 358–372. doi:10.1006/viro.2000.0530
  • Herniou, E. A., & Jehle, J. A. (2007). Baculovirus phylogeny and evolution. Current Drug Targets, 8, 1043–1050. doi:10.2174/138945007782151306
  • Herniou, E. A., Olszewski, J. A., Cory, J. S., & O'Reilly, D. R. (2003). The genome sequence and evolution of baculoviruses. Annual Review of Entomology, 48, 211–234. doi:10.1146/annurev.ento.48.091801.112756
  • Hoover, K., Kishida, K. T., DiGiorgio, L. A., Workman, J., Alaniz, S. A., & Hammock, B. D. (1998). Inhibition of baculoviral disease by plant-mediated peroxidise activity and free radical generation. Journal Chemical Ecology, 24, 1949–2001. doi:10.1023/A:1020777407980
  • Hu, Y. C. (2006). Baculovirus vectors for gene therapy. Advances in Virus Research, 68, 287–320.
  • Hunter, D. K., Hoffmann, D. F., & Collier, S. J. (1975). Observations on a granulosis virus of the potato tuber worm, Phthorimaea operculella. Journal of Invertebrate Pathology, 26, 397–400. doi:10.1016/0022-2011(75)90240-2
  • Ignoffo, C. M., & Garcia, C. (1966). The relation of pH to the activity of inclusion bodies of Heliothis nuclear polyhedrosis. Journal of Invertebrate Pathology, 8, 426–427. doi:10.1016/0022-2011(66)90064-4
  • Ignoffo, C. M., & Garcia, C. (1992). Combinations of environmental factors and simulated sunlight affecting activity of inclusion bodies of Heliothis (Lepidoptera: Noctuidae) nucleopolyhedrosis virus. Environmental Entomology, 21, 210–213.
  • Ignoffo, C. M., & Garcia, C. (1994). Antioxidant and oxidative enzyme effects on the inactivation of inclusion bodies of the Helilothis baculovirus by simulated sunlight-UV. Environmental Entomology, 23, 1025–1029.
  • Ignoffo, C. M., Garcia, C., & Saathoff, S. G. (1997). Sunlight stability and rain fastness of formulation of baculovirus Heliothis. Environmental Entomology, 26, 1470–1474.
  • Inceoglu, A. B., Kamita, S. G., & Hammock, B. D. (2006). Genetically modified baculoviruses: A historical overview and future outlook. Advances in Virus Research, 68, 323–360. doi:10.1016/S0065-3527(06)68009-3
  • Inceoglu, A. B., Kamita, S. G., Hinton, A. C., Huang, Q., Severson, T. F., Kang, K., & Hammock, B. D. (2001). Recombinant baculoviruses for insect control. Pest Management Science, 57, 981–987. doi:10.1002/ps.393
  • Jehle, J. A. (2008, February). The future of Cydia pomonella granulovirus in biological control of codling moth. Ecofruit – Proceedings to the 13th International Conference on Cultivation. Technique and Phytopathological Problems in Organic Fruit-Growing, Weinsberg, Germany. pp. 265–270.
  • Jehle, J. A., & Backhaus, H. (1994). The granulin gene region of Cryptophlebia leucotreta granulosis virus: Sequence analysis and phylogenetic considerations. Journal of General Virology, 75, 3667–3671. doi:10.1099/0022-1317-75-12-3667
  • Jehle, J. A., Backhaus, H., Fritsch, E., & Huber, J. (1992). Physical map of Cryptophlebia leucotreta granulosis virus genome and its relationship to the genome of Cydia pomonella granulosis virus. Journal of General Virology, 73, 1621–1626. doi:10.1099/0022-1317-73-7-1621
  • Jehle, J. A., Blissard, G. W., Bonning, B. C., Cory, J. S., Herniou, E. A., Rohrmann, G. F., & Vlak, J. M. (2006). On the classification and nomenclature of baculoviruses: A proposal for revision. Archives of Virology, 151, 1257–1266. doi:10.1007/s00705-006-0763-6
  • Jehle, J. A., Lange, M., Wang, H., Hu, Z. H., Wang, Y., & Hauschild, R. (2006). Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology, 346, 180–193. doi:10.1016/j.virol.2005.10.032
  • Jehle, J. A., Sayed, S. M., & Wahl-Ermel, B. (2006, July). What do we (need to) know about low-susceptibility of codling moth against Cydia pomonella gruanulovirus (CpGV). Ecofruit – Proceedings to the 12th International Conference on Cultivation. Technique and Phytopathological Problems in Organic Fruit-Growing, Weinsberg, Germany. pp. 14–18.
  • Jones, K. A., Cherry, A. J., & Grzywacz, D. (1997). Formulation: Is it an excuse for poor application?. In H. F. Evans (Ed.), Microbial insecticides: Novelty or necessity? (pp. 11–19). Farnham: Proc. Brit. Crop Prot. Council No. 68.
  • Jukes, M. D., Knox, C. M., Hill, M. P., & Moore, S. D. (2014). The isolation and genetic characterisation of a South African strain of Phthorimaea operculella granulovirus. Virus Research, 183, 85–88. doi:10.1016/j.virusres.2014.01.013
  • Kadir, H. B. A., Payne, C. C., Crook, N. E., & Winstanley, D. (1999). Characterization and cross-transmission of baculoviruses infectious to the diamondback moth, Plutella xylostella, and some other lepidopteran pests of brassica crops. Biocontrol Science Technology, 9, 227–238. doi:10.1080/09583159929802
  • Kawarakata, T., Funakoshi, M., & Aratake, Y. (1980). Purification and properties of the Bombyx mori polyhedrosis virus liberated from polyhedral by dissolution with silkworm gut juice. Journal of Invertebrate Pathology, 35, 34–42. doi:10.1016/0022-2011(80)90080-4
  • Kessler, P., & Zingg, D. (2008, July 6–12). New baculovirus products offer solutions for the biological control of Cydia pomonella and Cryptophlebia leucotreta. Proceedings of the 23rd International Congress of Entomology, Pest Management: Perennial Crops, Durban, South, Africa.
  • Kfir, R. (2003). Biological control of the potato tuber moth Phthorimaea operculella in Africa. Biological control in IPM systems in Africa. Cotonou: CABI. pp. 77–85.
  • Kienzle, J., Zebitz, C. P. W., Zimmer, J., & Volk, F. (2007, March). Initial field tests for effect of Madex plus against CpGV-resistant codling moth populations in Ojo-enterprises. Contributions to the 9th scientific conference on organic agriculture. vol. 1, pp. 297–300, University of Hohenheim, Germany.
  • Kirkman, W. (2007). Understanding and improving the residual efficacy of the Cryptophlebia leucotreta granulovirus (CRYPTOGRAN) ( MSc thesis). Rhodes University, Grahamstown, South Africa. 115 pp.
  • Klein, H., Hill, M. P., Zachariades, C., & Zimmermann, H. G. (2011). Regulation and risk assessment for importations and releases of biological control agents against invasive alien plants in South Africa. African Entomology, 19, 488–497. doi:10.4001/003.019.0215
  • Knight, A. L., Brunner, J. F., & Alston, D. (1994). Survey of azinphosmethyl resistance in codling moth (Lepidoptera: Tortricidae) in Washington and Utah. Journal of Economic Entomology, 87, 285–292.
  • Kost, T. A., Condreay, J. P., & Jarvis, D. L. (2005). Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nature Biotechnology, 23, 567–575. doi:10.1038/nbt1095
  • Krawczyk, G., Hull, L. A., & Bohnenblust, E. (2010). Utilization of mating disruption and codling moth granulovirus (CmGV) in conventional commercial apple orchards in Pennsylvania USA. IOBC/WPRS Bulletin, 54, 71–74.
  • Kroemer, J. A., & Webb, B. A. (2004). Polydnavirus genes and genomes: Emerging gene families and new insights into polydnavirus replication. Annual Review of Entomology, 49, 431–456. doi:10.1146/annurev.ento.49.072103.120132
  • Kroschel, J., & Koch, W. (1994). Studies on the population dynamics of the potato tuber moth (Phthorimaea operculella Zell. (Lep., Gelechiidae) in the Republic of Yemen. Journal of Applied Entomology, 118, 327–341. doi:10.1111/j.1439-0418.1994.tb00808.x
  • Kroschel, J., & Lacey, L. A. (Eds.). (2008). “Integrated Pest Management for the Potato Tuber Moth, Phthorimaea operculella (Zeller) – a Potato Pest of Global Importance.” Tropical Agriculture, 20, 147. Advances in Crop Research 10. Weikersheim: Margraf Verlag.
  • Laarif, A., Fattouch, S., Essid, W., Marzouki, N., Salah, H. B., & Hammouda, M. H. B. (2003). Epidemiological survey of Phthorimaea operculella granulosis virus in Tunisia. Bulletin OEPP, 33, 335–338. doi:10.1046/j.1365-2338.2003.00656.x
  • Lacey, L. A., & Arthurs, S. P. (2008). An overview of microbial control of the potato tuber moth. In J. Kroschel & L. Lacey (Eds.), Integrated pest management for the potato tuber moth, Phthorimaea operculella (Zeller)a potato pest of global importance. Tropical agriculture (p. 20). Advances in Crop Research 10. Weikersheim: Margraf.
  • Lacey, L. A., Frutos, R., Kaya, H. K., & Vail, P. (2001). Insect pathogens as biological control agents: Do they have a future? Biological Control, 21, 230–248. doi:10.1006/bcon.2001.0938
  • Lacey, L. A., & Kroschel, J. (2009). Microbial control of the potato tuber moth (Lepidoptera: Gelechiidae). Fruit, Vegetable, and Cereal Science and Biotechnology, 3 (Special Year of the Potato Issue 1), 46–54.
  • Lacey, L. A., Thomson, D., Vincent, C., & Arthurs, S. P. (2008). Codling moth granulovirus: A comprehensive review. Biocontrol Science and Technology, 18, 639–663. doi:10.1080/09583150802267046
  • Lange, M., & Jehle, J. A. (2003). The genome of the Cryptophlebia leucotreta granulovirus. Virology, 317, 220–236. doi:10.1016/S0042-6822(03)00515-4
  • Lapointe, R., Thumbi, D., & Lucarotti, C. J. (2012). Recent advances in our knowledge of baculovirus molecular biology and its relevance for the registration of baculovirus-based products for insect pest population control, integrated pest management and pest control - current and future tactics (S. Soloneski, ed.). InTech. Retrieved from http://www.intechopen.com/books/integrated-pest-management-and-pest-control-current-and-futuretactics/recent-advances-in-our-knowledge-of-baculovirus-molecular-biology-and-its-relevance-for-the-registra
  • Luque, T., Finch, R., Crook, N. E., O'Reilly, D. R., & Winstanley, D. (2001). The complete sequence of the Cydia pomonella granulovirus genome. Journal of General Virology, 82, 2531–2547.
  • Maeda, S. (1989). Increased insecticidal effect by a recombinant baculovirus carrying a synthetic diuretic hormone gene. Biochemical and Biophysical Research Communications, 165, 1177–1183.
  • Mascarin, G. M., Alves, S. B., Ferreira, F. T. R., Urbano, M. R., Demétrio, C. G. B., & Delalibera, I. (2010). Potential of a granulovirus isolate to control Phthorimaea operculella (Lepidoptera: Gelechiidae). BioControl, 55, 657–671. doi:10.1007/s10526-010-9277-y
  • McGuire, M. R., Behle, R. W., Goebel, H. N., & Fry, T. C. (2000). Calibration of a sunlight simulator for determining solar stability of Bacillus thuringiensis and Anagrapha flacifera nuclear polyhedrovirus. Environmental Entomology, 29, 1070–1074. doi:10.1603/0046-225X-29.5.1070
  • Mertens, P. P. C., Duncan, R., Attoui, H., & Dermody, T. S. (2005). Reoviridae. In C. M. Fauguet, M. A. Mayo, J. Maniloff, U. Desselberger, & L. A. Ball (Eds.), Virus taxonomy. Eighth report of the international committee on taxonomy of viruses (pp. 447–454). Amsterdam: Elsevier.
  • Miller, L. K. (1997). The baculoviruses. New York, NY: Plenum. 447 pp.
  • Mishra, S. (1998). Baculoviruses as pesticides. Current Science, 75, 1015–1022.
  • Moore, S. D. (2002). The development and evaluation of Cryptophlebia leucotreta granulovirus (CrleGV) as a biological control agent for the management of the false codling moth, Cryptophlebia leucotreta, on citrus ( PhD thesis). Rhodes University, Grahamstown, 311 pp.
  • Moore, S., & Kirkman, W. (2010). Helicovir™: A virus for the biological control of bollworm. South African Fruit Journal, 9, 63–67.
  • Moore, S., Kirkman, W., & Stephen, P. (2004). Cryptogran. A virus for the biological control of false codling moth. South African Fruit Journal, 3, 35–39.
  • Moore, S. D., Hendry, D. A., & Richards, G. I. (2011). Virulence of a South African isolate of the Cryptophlebia leucotreta granulovirus to Thaumatotibia leucotreta neonate larvae. BioControl, 56, 341–352. doi:10.1007/s10526-010-9339-1
  • Moore, S. D., Pittaway, T., Bouwer, G., & Fourie, J. G. (2004). Evaluation of Helicoverpa armigera nucleopolyhedrovirus, HearNPV, for control of Helicoverpa armigera Hübner (Noctuidae: Lepidoptera) on citrus in South Africa. Biocontrol Science and Technology, 14, 239–250.
  • Moore, S. D., Richards, G. I., Chambers, C., & Hendry, D. (2014). An improved larval diet for commercial mass rearing of the false codling moth, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae). African Entomology, 22, 216–219.
  • Morales, L., Moscardi, F., Sosa-Gomez, D. R., Paro, F. E., & Soldorio, I. L. (2001). Fluorescent brighteners improve Anticarsia gemmatalis (Lepidoptera: Noctuidae) nucleopolyhedrovirus (AgMNPV) activity on AgMNPV susceptible and resistant strains of insect. Biological Control, 20, 247–253. doi:10.1006/bcon.2000.0904
  • Moran, V. C. (1983). The phytophagous insects and mites of cultivated plants in South Africa: Patterns and pest status. Journal of Applied Ecology, 20, 439–450. doi:10.2307/2403518
  • Moscardi, F. (1999). Assessment of the application of baculoviruses for control of Lepidoptera. Annual Review of Entomology, 44, 257–289. doi:10.1146/annurev.ento.44.1.257
  • Moscardi, F., de Souza, M. L., de Castro, M. E. B., Moscardi, M. L., & Szewczyk, B. (2011). Baculovirus pesticides: Present state and future perspectives. In I. Ahmad, F. Ahmad, & J. Pichtel (Eds.), Microbes and microbial technology: Agricultural and environmental applications (pp. 415–445). New York Dordrecht Heidelberg London: © Springer Science+Business Media, LLC.
  • Mota-Sánchez, D., Wise, J. C., Poppen, R. V., Gut, L. J., & Hollingworth, R. M. (2008). Resistance of codling moth, Cydia pomonella (L) (Lepidoptera: Tortricidae), larvae in Michigan to insecticides with different modes of action and the impact on field residual activity. Pest Management Science, 64, 881–890. doi:10.1002/ps.1576
  • Mück, O. (1985). Biologie, verhalten und wirtshcaftliche bedeutaung von parasiten schädlicher Lepidopteren auf den Kapverden [Biology, behaviour and economic impact of noxious lepidopteran parasites on the Cape Verde islands]. Neue Entomologische Nachrichten, 18, 168.
  • Murphy, F. A., Fauquet, C. M., Bishop, D. H. L., Ghabrial, S. A., Jarvis, A. W., Martelli, G. P., & Summers, M. D. (Eds.). (1995). Virus taxonomythe classification and nomenclature of viruses: Sixth report of the international committee on taxonomy of viruses (pp. 1–586). New York: Springer-Verlag.
  • Muthamia, E. K., Ogada, P. A., Mukunzu, M. J., Vanbeek, N. A. M., Wesonga, J. M., & Ateka, E. M. (2011). Characterization of Plutella xylostella granulovirus (PlxyGV) isolates for the management of diamondback moth in Kenya. African Journal of Horticultural Sciences, 4, 19–23.
  • Newton, P. J. (1998). False codling moth Cryptophlebia leucotreta (Meyrick). In E. C. G. Bedford, M. A. Van den Berg, & E. A. De Villiers (Eds.), Citrus pests in the Republic of South Africa (pp. 192–200). Nelspruit: Dynamic Ad.
  • Oerke, E. C. (2006). Crop losses to pests. Journal of Agricultural Science, 144, 31–43.
  • Ogembo, J. G. (2002). Comparative biological and biochemical studies of two isolates of nucleopolyhedroviruses infecting Helicoverpa armigera Hübner (Lepidoptera: Noctuidae) ( Thesis: Master of Science in tropical entomology). University of Zimbabwe, Harare, 112 pp.
  • Opoku-Debrah, J. K., Hill, M. P., Knox, C., & Moore, S. D. (2013). Overcrowding of false codling moth, Thaumatotibia leucotreta (Meyrick) leads to the isolation of five new Cryptophlebia leucotreta granulovirus (CrleGV-SA) isolates. Journal of Invertebrate Pathology, 112, 219–228. doi:10.1016/j.jip.2012.12.008
  • Opoku-Debrah, J. K., Hill, M. P., Knox, C., & Moore, S. D. (2014). Comparison of the biology of geographically distinct populations of the citrus pest, Thaumatotibia leucotreta (Meyrick) (Lepidoptera: Tortricidae), in South Africa. African Entomology, 22.
  • O'Reilly, D. R., Kelly, T. J., Masler, E. P., Thyagaraja, B. S., Robson, R. M., Shaw T. C., & Miller, L. K. (1995). Overexpression of Bombyx mori prothoracicotropic hormone using baculovirus vectors. Insect Biochemistry and Molecular Biology, 25, 45–85.
  • O'Reilly, D. R., & Miller, L. K. (1991). Improvement of a buculovirus pesticide by deletion of the egt gene. Bio/Technology, 9, 1086–1089. doi:10.1038/nbt1191-1086
  • Parnell, M., Grzywacz, D., Jones, K. A., & Brown, M. (2002). The strain variation and virulence of granulovirus of diamondback moth (Plutella xylostella Linnaeus, Lep., Yponomeutidae) isolated in Kenya. Journal of Invertebrate Pathology, 79, 192–196. doi:10.1016/S0022-2011(02)00001-0
  • Pasarelli, A. L. (2011). Barriers to success: How baculoviruses establish efficient systematic infections. Virology, 411, 382–392. ISSN 0042-6822. doi:10.1016/j.virol.2011.01.009
  • Pidre, M. L., Ferrelli, M. L., Haase, S., & Romanowski, V. (2013). Baculovirus display: A novel tool for vaccination, current issues in molecular virology - viral genetics and biotechnological applications (V. Romanowski, ed.). ISBN: 978-953-51-1207-5. InTech. Retrieved from http://www.intechopen.com/books/current-issues-in-molecular-virology-viral-genetics-and-biotechnological-applications/baculovirus-display-a-novel-tool-for-vaccination
  • Pringle, K. L., Eyles, D. K., & Brown, L. (2003). Trends in codling moth activity in apple orchards under mating disruption using pheromones in the Elgin area, Western Cape Province, South Africa. African Entomology, 11, 65–75.
  • Rabindra, R. J., Geetha, N., Renuka, S., Varadharajan, S., & Regupathy, A. (1997). Occurrence of a granulosis virus from two populations of Plutella xylostella (L.) in India. Proceedings Third International MARDI Workshop, 1996, Kuala Lumpur, Malaysia. pp. 113–115.
  • Raman, K. V. (1994). Pest management in developing countries. In G. W. Zehnder, M. L. Powelson, R. K. Jansson, & K. V. Raman (Eds.), Advances in potato pest biology and management (pp 583–596). St. Paul, MN: The American Phytopathological Society Press.
  • Raman, K. V., & Alcázar, J. (1988, June 16–25). Biological control of potato tuber moth, Phthorimaea operculella, using a granulosis virus in Peru. Proceedings of the Asian Potato Association, Kuming, China. pp. 173–174.
  • Reed, E. M. (1969). A granulosis virus of potato moth. Australian Journal of Science, 31, 300–301.
  • Reuveny, H., & Cohen, E. (2004). Resistance of the codling moth Cydia pomonella (L) (Lep., Tortricidae) to pesticides in Israel. Journal of Applied Entomology, 128, 645–651. doi:10.1111/j.1439-0418.2004.00901.x
  • Reyes, M., Franck, P., Charmillot, P.-J., Ioriatti, C., Olivares, J., Pasqualini, E., & Sauphanor, B. (2007). Diversity of insecticide resistance mechanisms and spectrum in European populations of the Codling moth, Cydia pomonella. Pest Management Science, 63, 890–902. doi:10.1002/ps.1421
  • Rezapanah, M., Shojai-Estabragh, S., & Jehle, J. A. (2008). Molecular and biological characterization of new isolates of Cydia pomonella granulovirus from Iran. Journal of Pest Science, 81, 187–191. doi:10.1007/s10340-008-0204-2
  • Rodriguez, V. A., Belaich, M. N., & Ghiringhelli, P. D. (2012). Baculoviruses: Members of integrated pest management strategies, integrated pest management and pest control – current and future tactics (S. Soloneski, ed.), ISBN: 978-953-51-0050-8. InTech. Retrieved from http://www.intechopen.com/books/integrated-pest-management-and-pest-control-current-and-futuretactics/baculoviruses-members-of-integrated-pest-management-strategies
  • Rohrmann, G. F. (1986). Polyhedrin structure. Journal General Virology, 67, 1499–1513. doi:10.1099/0022-1317-67-8-1499
  • Rohrmann, G. F. (2011). Baculovirus molecular biology: Second edition. National Library of Medicine (US), National Center for Biotechnology Information. Retrieved from http://www.ncbi.nlm.nih.gov/books/NBK49500/
  • Rohrmann, G. F. (2013). Baculovirus molecular biology: Third edition. National Library of Medicine (US), National Center for Biotechnology Information. Retrieved from http://www.ncbi.nlm.nih.gov/books/NBK114593/
  • Sarfraz, M., Keddie, A. B., & Dosdall, L. M. (2005). Biological control of the diamondback moth, Plutella xylostella: A review. Biocontrol Science and Technology, 15, 763–789. doi:10.1080/09583150500136956
  • Sauphanor, B., Berling, M., Toubon, J.-F., Reyes, M., Delnatte, J., & Allenoz, P. (2006). Carpocapse des pommes. cas de résistance au virus de la granulose en vergers biologique [The case of resistance to the granulosis virus in biological tests]. Phytoma, 590, 24–27.
  • Sauphanor, B., Bouvier, J. C., & Brosse, V. (1998). Spectrum of insecticide resistance in Cydia pomonella (Lepidoptera: Tortricidae) in southeastern France. Journal of Economic Entomology, 91, 1225–1231.
  • Setiawati, W., Soeriaatmadja, R. E., Rubiati, T., & Chujoy, E. (1999). Control of potato tubermoth (Phthorimaea operculella) using an indigenous granulosis virus in Indonesia. Indonesian Journal of Crop Science, 14, 10–16.
  • Shapiro, M., Agin, P. P., & Bell, R. A. (1983). Ultraviolet protectants of the gypsy moth (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus. Environmental Entomology, 12, 982–985.
  • Shel'Deshova, G. G. (1967). Ecological factors determining the distribution of the codling moth Laspeyresia pomonella L (Lepidoptera, Tortricidae) in the northern and southern hemispheres. Entomological Review, 46, 349–361.
  • Singh, S., Moore, S. D., Spillings, B., & Hendry, D. (2003). Characterization of a South African isolate of Cryptophlebia leucotreta granulovirus. Journal of Invertebrate Pathology, 83, 249–252. doi:10.1016/S0022-2011(03)00081-8
  • Souza, M. L., Castro, M. E. B., de Sihler, W., Krol, E., & Szewczk, B. (2007). Baculoviruses: A safe alternative in pest control? Pest Technology, 1, 53–60.
  • Sporleder, M. (2003). The granulovirus of the potato tuber moth Phthorimaea operculella (Zeller): Characterization and prospects for effective mass production and pest control. In J. Kroschel (Ed.), Tropical agriculture – advances in crop research (3) (pp. 206). Weikersheim: Margraf Verlag.
  • Stern, V. M., Smith, R. F., van den Bosch, R., & Hagen, K. S. (1959). The integration of chemical and biological control of the spotted alfalfa aphid. The integrated control concept. Hilgardia, 29, 81–101.
  • Sun, X., & Peng, H. (2007). Recent advances in biological control of pest insects by using viruses in China. Virologica Sinica, 22, 158–162. doi:10.1007/s12250-007-0017-0
  • Sun, X., Wang, H., Sun, X., Chen, X., Peng, C., Pan, D., & Hu, Z. (2004). Biological activity and field efficacy of a genetically modified Helicoverpa armigera single-nucleocapsid nucleopolyhedrovirus expressing an insect-selective toxin from a chimeric promoter. Biological Control, 29, 124–137. doi:10.1016/S1049-9644(03)00117-8
  • Szewczyk, B., de Souza, M. L., de Castro, M. E. B., Moscardi, M. L., & Moscardi, F. (2011). Baculovirus biopesticides. In M. Stoytcheva (Ed.), Pesticides, formulation, effects, fate (pp. 25–36). Rijeka: InTech Open Access. ISBN: 978-953-307-532-7.
  • Szewczyk, B., Hoyos-Carvajal, L., Paluszek, M., Skrzecz, I., & de Souza, M. L. (2006). Baculovirus re-emerging biopesticides. Biotechnology Advances, 24, 143–160. doi:10.1016/j.biotechadv.2005.09.001
  • Szewczyk, B., Rabalski, L., Krol, E., Sihler, W., & de Souza, M. L. (2009). Baculovirus biopesticides – a safe alternative to chemical protection of plants. Journal of Biopesticides, 2, 209–216.
  • Talekar, N. S., & Shelton, A. M. (1993). Biology, ecology, and management of diamondback moth. Annual Review of Entomology, 38, 275–301. doi:10.1146/annurev.en.38.010193.001423
  • Tanada, Y. (1964). A granulosis virus of the codling moth, Carpocapsa pomonella (Linnaeus) (Olethreutidae, Lepidoptera). Journal of Invertebrate Pathology, 6, 378–380.
  • Theilmann, D. A., Blissard, G. W., Bonning, B., Jehle, J., O'Reilly, D. R., Rohrmann, G. F., & Vlak, J. M. (2005). Baculoviridae. In C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger, & L. A. Ball (Eds.), Virus taxonomy, eighth report of the international committee on taxonomy of viruses (pp. 177–185). London: Elsevier/Academic Press.
  • van Oers, M. M., & Vlak, J. M. (1997). The baculovirus 10-kDa protein. Journal of Invertebrate Pathology, 70, 1–17. doi:10.1006/jipa.1997.4675
  • Vergnani, S., Caruso, S., Boselli, M., & Pasqualini, E. (2008, June 18–20). Efficacy of Cydia pomonella granulovirus (CpGV) in controlling moth in the Emilia-Romagna region. 2nd Conference of the International Society of Organic Agriculture Research ISOFAR, Modena, Italy. Retrieved from http://orgprints.org/12189/
  • Vermeulen, J. B., & Bedford, E. C. G. (1998). American bollworm, Helicoverpa (=Heliothis) armigera (Hübner). In E. C. G. Bedford, M. A. Van den Berg, & E. A. De Villiers (Eds.), Citrus Pests in the Republic of South Africa (2nd ed. (revised), pp. 217–221). Pretoria: Dynamic Ad.
  • Vincent, C. M., Andermatt, M., & Valero, J. (2007). Madex and virosoft, viral biopesticides for codling moth control. In C. Vincent, M. S. Goettel, & G. Lazarovits (Eds.), Biological control: A global perspective (pp. 336–343). Wallingford: CAB International.
  • Wearing, C. H., Hansen, J. D., Whyte, C., Miller, C. E., & Brown, J. (2001). The potential for spread of codling moth (Lepidoptera: Tortricidae) via commercial sweet cherry fruit: A critical review and risk assessment. Crop Protection, 20, 465–488. doi:10.1016/S0261-2194(01)00023-0
  • Whitlock, V. H. (1974). Symptomatology of two viruses infecting Heliothis armigera. Journal of Invertebrate Pathology, 23(1), 70–75. doi:10.1016/0022-2011(74)90075-5
  • Wormleaton, S. L., & Winstanley, D. (2001). Phylogenetic analysis of conserved genes within the ecdysteroid UDP-glucosyltransferase gene region of the slow-killing Adoxophyes orana granulovirus. Journal of General Virology, 82, 2295–2305.
  • Wright, D. (2004). Biological control of DBM: A global perspective. In D. Bordat & A. A. Kirk (Eds.), Improving biocontrol of Plutella xylostella (pp. 9–14). Montpellier: CIRAD. ISBN 2-87614 570 7. Proceedings of the International Symposium in Montpellier, France, 21–24 Oct 2002.
  • Yang, M. M., Li, M. L., Zhang, Y. A., Wang, Y. Z., Qu, L. J., Wang, Q. H., & Ding, J. Y. (2012). Baculoviruses and insect pest control in China. African Journal of Microbiology Research, 6, 214–218. doi:10.5897/AJMR12.1123
  • Zalucki, M. P., Shabbir, A., Silva, R., Adamson, D., Liu, S. S., & Furlong, M. J. (2012). Estimating the economic cost of one of the world's major insect pests, Plutella xylostella: Just how long is a piece of string? Journal of Economic Entomology, 105, 1115–1129. doi:10.1603/EC12107
  • Zeddam, J. L., Pollet, A., Mangoendiharjo, S., Ramadhan, T. H., & Lopez-Ferber, M. (1999). Occurrence and virulence of a granulosis virus in Phthorimaea operculella (Lep. Gelechiidae) populations in Indonesia. Journal of Invertebrate Pathology, 74, 48–54. doi:10.1006/jipa.1998.4840
  • Zingg, D., & Kessler, P. (2008). Madex plus and Madex I12 break virus resistance of codling moth. Andermatt Group Publication, 15, 7–10.
  • Zingg, D., Zuger, M., Bollhalder, F., & Andermatt, M. (2011). Use of resistance overcoming CpGV isolates and CpGV resistance situation of the codling moth in Europe seven years after the first discovery of resistance to CpGV-M. IOBC/wprs Bulletin, 66, 401–404.
  • Zou, Y., & Young, S. Y. (1994). Enhancement of nuclear polyhedrosis virus activity in larval pests of Lepidoptera by a stilbene fluorescent brightener. Journal of Entomological Science, 29, 130–133.

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