This article was downloaded by: [USDA National Agricultural Library] On: 28 October 2008 Access details: Access Details: [subscription number 790740294] Publisher Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Biocontrol Science and Technology Publication details, including instructions for authors and subscription information: http://www.informaworld.com/smpp/title~content=t713409232 Codling moth granulovirus: a comprehensive review Lawrence A. Lacey a; Donald Thomson b; Charles Vincent c; Steven P. Arthurs d a Yakima Agricultural Research Laboratory, USDA-ARS, Wapato, WA, USA b DJS Consulting Services, Seattle, WA, USA c Centre de recherche et de développement en horticulture, Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, QC, Canada d Department of Entomology and Nematology, University of Florida, IFAS, Mid Florida Research and Education Center, Apopka, FL, USA First Published on: 13 August 2008 To cite this Article Lacey, Lawrence A., Thomson, Donald, Vincent, Charles and Arthurs, Steven P.(2008)'Codling moth granulovirus: a comprehensive review',Biocontrol Science and Technology,18:7,639 — 663 To link to this Article: DOI: 10.1080/09583150802267046 URL: http://dx.doi.org/10.1080/09583150802267046 PLEASE SCROLL DOWN FOR ARTICLE Full terms and conditions of use: http://www.informaworld.com/terms-and-conditions-of-access.pdf This article may be used for research, teaching and private study purposes. Any substantial or systematic reproduction, re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expressly forbidden. The publisher does not give any warranty express or implied or make any representation that the contents will be complete or accurate or up to date. The accuracy of any instructions, formulae and drug doses should be independently verified with primary sources. The publisher shall not be liable for any loss, actions, claims, proceedings, demand or costs or damages whatsoever or howsoever caused arising directly or indirectly in connection with or arising out of the use of this material. Biocontrol Science and Technology, Vol. 18, No. 7, 2008, 639Á663 REVIEW Codling moth granulovirus: a comprehensive review Lawrence A. Laceya*, Donald Thomsonb, Charles Vincentc and Steven P. Arthursd aYakima Agricultural Research Laboratory, USDA-ARS, Wapato, WA, USA; bDJS Consulting Services, Seattle, WA, USA; cCentre de recherche et de de´veloppement en horticulture, Agriculture et Agroalimentaire Canada, Saint-Jean-sur-Richelieu, QC, Canada; dDepartment of Entomology and Nematology, University of Florida, IFAS, Mid Florida Research and Education Center, Apopka, FL, USA (Received 25 March 2008; returned 16 May 2008; accepted 10 June 2008) Codling moth (CM), Cydia pomonella (L), is regarded as the most serious insect pest of apple worldwide. A variety of problems associated with the traditional use of non- selective insecticides for its control include: untoward environmental effects, insecticide resistance, negative impacts on natural enemies, and safety for pesticide applicators and the food supply. Concerns about these consequences have increased the interest in and development of alternative means for CM control that have little or no impact on humans, beneficial organisms and sensitive ecosystems. An effective and selective alternative to chemical insecticides for CM control is the CM granulovirus (CpGV). The virus was first isolated in Mexico and subsequently studied and evaluated in Europe and North America. A variety of research including pathology, pathogenesis and histo- pathology of the virus, determination of virulence, development of production methods, field use, factors that influence efficacy, commercial development, formulation, and CM resistance to the virus has been conducted. Commercial products of CpGV are now produced in Europe and North America and used by orchardists worldwide. In this paper we present a comprehensive review of the CpGV literature and the role of the virus in integrated pest management. Keywords: codling moth; Cydia pomonella; granulovirus; resistance; pathology; commercial development; integrated pest management Introduction Codling moth (CM), Cydia pomonella (L), (Lepidoptera: Tortricidae) is a serious pest of pome fruit (apple pear, crab apple, quince) and walnuts and can also survive in alternative Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 hosts, such as hawthorn (Crataegus spp.). CM is regarded as the most injurious insect pest of apple in most countries where apple is grown (Barnes 1991). It is usually controlled in conventional orchards with broad-spectrum insecticides such as azinphos-methyl † (Guthion ). Extensive use of broad spectrum pesticides has resulted in a variety of problems including negative environmental effects, insecticide resistance, outbreaks of secondary pests due to disruption of natural controls, and safety of pesticide applicators and the food supply. These concerns have increased the interest in and development of alternative means of control that have lower or no impact on beneficial organisms and *Corresponding author. Email: [email protected] First published online 13 August 2008 ISSN 0958-3157 print/ISSN 1360-0478 online This material is declared a work of the United States Goverment and is not subject to copyright protection: approved for public release; distribution is unlimited. DOI: 10.1080/09583150802267046 http://www.informaworld.com 640 L.A. Lacey et al. sensitive ecosystems (Lacey and Shapiro-Ilan 2008). An effective alternative to non- selective chemical insecticides with no impact on beneficial organisms is the CM granulovirus (CpGV). In this review, we will provide comprehensive background on the virus and its potential for incorporation into integrated pest management (IPM) in orchard agroecosystems. Description, pathogenesis, histopathology and transmission of CpGV CpGV was originally isolated from infected CM larvae collected near Valle de Allende, Chihuahua, Mexico and described by Tanada (1964). CpGV is the type species for the genus Granulovirus within the family Baculoviridae (Theilmann et al. 2005; Jehle et al. 2006), and as such has a circular, double-stranded DNA genome and has both budded and occluded virus phenotypes (Crook, Spencer, Payne, and Leisy 1985; Crook 1986; Tanada and Hess 1991; Federici 1997). Granuloviruses are so named because of their granular appearance under high magnification in light microscopy. The granules, also referred to as occlusion bodies (OBs), consist of a viral encoded protein (granulin) matrix in which a single rod-shaped, enveloped virion is occluded (Federici 1986; Tanada and Hess 1991). The nucleocapsid consists of a protein coat containing the viral DNA genome (Figure 1). CpGV OBs are ovocylindrical and approximately 360 190 nm wide (based on measure of micrographs in Tanada 1964). Electron microscopy studies of the fine structure of the virus have also been reported by Stairs, Parrish, Briggs, and Allietta (1966), Tanada and Leutenegger (1968), and Hess and Falcon (1987) and its structure is typical of other granuloviruses (Federici 1986). CpGV is one of the most virulent granuloviruses, categorised as a type 2 granulovirus which is faster acting than types 1 or 3, with a broader range of tissues infected and resulting rupture of the integument. (Tanada and Hess 1991; Federici 1997). The OBs must Downloaded By: [USDA National Agricultural Library] At: 21:32 28 October 2008 Figure 1. Electron micrographs of the nucleocapsid and occlusion bodies (OBs) of the codling moth granulovirus. (A) shows a longitudinal section of the nucleocapsid. The (a) end of nucleocapsid orients toward the plasma membrane during the budding process while the (P) end is blunt and striated. The core (C) contains DNA and protein. (B) shows two OBs in cross-section. (N) is the capsid and core (Z) is an amorphous zone and membrane (M). The majority of the OB is a matrix of granulin. (L) indicates the outer envelop. Both bars are equal to 100 nm. Micrographs are from Tanada and Hess (1991). Copyright 1991. Reprinted with permission by CRC Press. Biocontrol Science and Technology 641 be consumed by larvae in order to produce infections. When neonate larvae ingest a lethal concentration of the virus, death ensues in as few as 3 days (Glen and Clark 1985; Brain and Glen 1989; Ballard, Ellis, and Payne 2000b; Lacey, Vail, and Hoffmann 2002). The LD50 has been estimated as low as 1.2Á5 OBs per neonate larva (Sheppard and Stairs 1977; Harvey and Volkman 1983; Huber 1986) with higher estimates for number of OBs/mm2 of artificial diet (Laing and Jaques 1980; Huber 1981; Eastwell, Cossentine, and Bernardy 1999; Lacey et al. 2002). Older instars require higher doses of the virus (Keller 1973; Sheppard and Stairs 1977; Camponovo and Benz 1984). When older CM larvae are fed low dosages of the virus, they have a higher and longer rate of weight increase than uninfected larvae (Jans and Benz 1985). Following ingestion, the proteinaceous coat or granulin is dissolved in the alkaline pH of the midgut liberating the nucleocapsids. The nucleocapsids pass through the peritrophic membrane and then fuse with the microvilli of the midgut epithelium. After entering the cells, the nucleocapsids are transported to the nuclear membrane where the viral DNA genome appears to enter the nucleus by way of the nuclear pore.