Progressive Adaptation of a CpGV Isolate to Codling Moth Populations Resistant to CpGV-M

Graillot, Benoît; Berling, Marie; Blachère-López, Christine; Siegwart, Myriam; Besse, Samantha; López‐Ferber, M.

doi:10.3390/v6125135

Cited by 19 publications

(35 citation statements)

References 16 publications

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“…For CpRR1, it was demonstrated that resistance-breaking properties of the CpGV isolates depended on the lack of an insertion of 24 bp in the open reading frame (ORF) pe38 in CpGV-M (group A), which is missing in all resistance-breaking isolates of genome group B to E CpGVs (6). By registration of some of these isolates, a successful commercial control of the type I resistance in C. pomonella was eventually reestablished in Europe (23)(24)(25)(26)(27)(28).…”

Section: Importancementioning

confidence: 99%

A Third Type of Resistance to Cydia pomonella Granulovirus in Codling Moths Shows a Mixed Z-Linked and Autosomal Inheritance Pattern

Schulze-Bopp

Fritsch

et al. 2017

Appl Environ Microbiol

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Different isolates of Cydia pomonella granulovirus (CpGV) are used worldwide to control codling moth larvae () in pome fruit production. Two types of dominantly inherited field resistance of to CpGV have been recently identified: Z-chromosomal type I resistance and autosomal type II resistance. In the present study, a CpGV-resistant field population (termed SA-GO) from northeastern Germany was investigated. SA-GO individuals showed cross-resistance to CpGV isolates of genome group A (CpGV-M) and genome group E (CpGV-S), whereas genome group B (CpGV-E2) was still infective. Crossing experiments between individuals of SA-GO and the susceptible strain CpS indicated the presence of a dominant autosomal inheritance factor. By single-pair inbreeding of SA-GO individuals for two generations, the genetically more homogenous strain CpRGO was generated. Resistance testing of CpRGO neonates with different CpGV isolates revealed that isolate CpGV-E2 and isolates CpGV-I07 and -I12 were resistance breaking. When progeny of hybrid crosses and backcrosses between individuals of resistant strain CpRGO and susceptible strain CpS were infected with CpGV-M and CpGV-S, resistance to CpGV-S appeared to be autosomal and dominant for larval survivorship but recessive when success of pupation of the hybrids was considered. Inheritance of resistance to CpGV-M, however, is proposed to be both autosomal and Z linked, since Z linkage of resistance was needed for pupation. Hence, we propose a further type III resistance to CpGV in, which differs from type I and type II resistance in its mode of inheritance and response to CpGV isolates from different genome groups. The baculovirus Cydia pomonella granulovirus (CpGV) is registered and applied as a biocontrol agent in nearly all pome fruit-growing countries worldwide to control codling moth caterpillars in an environmentally friendly manner. It is therefore the most widely used commercial baculovirus biocontrol agent. Since 2005, field resistance of codling moth to CpGV products has been observed in more than 40 field plantations in Europe, threatening organic and integrated apple production. Knowledge of the inheritance and mechanism(s) of resistance is indispensable for the understanding of host response to baculovirus infection on the population level and the coevolutionary arms race between virus and host, as well as for the development of appropriate resistance management strategies. Here, we report a codling moth field population with a new type of resistance, which appears to follow a highly complex inheritance in regard to different CpGV isolates.

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Section: Importancementioning

confidence: 99%

A Third Type of Resistance to Cydia pomonella Granulovirus in Codling Moths Shows a Mixed Z-Linked and Autosomal Inheritance Pattern

Schulze-Bopp

Fritsch

et al. 2017

Appl Environ Microbiol

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“…It was expected that CpGV resistance in other regions in Europe would follow a mode similar to that of CpRR1, because (i) a Z-chromosomal dominant inheritance was determined for several widely separated CM populations in Germany, France, and the Czech Republic (13,19,25,26); and (ii) the resistant CM populations in Europe were susceptible to resistance-breaking CpGV isolates, several of which have been registered and used as new CpGV products in Europe (10,21,22,(27)(28)(29)(30).…”

mentioning

confidence: 99%

Evidence for a Second Type of Resistance against Cydia pomonella Granulovirus in Field Populations of Codling Moths

Jehle

Schulze-Bopp

Undorf-Spahn

et al. 2017

Appl Environ Microbiol

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Cydia pomonella granulovirus (CpGV) is an important biocontrol agent for the codling moth (CM) in organic and integrated apple production worldwide. Previously, Z chromosome-linked dominant resistance in at least 38 CM field populations in Europe was reported, threatening organic apple production. Growers responded by switching to a different resistance-breaking isolate of CpGV that could control these populations. Here, we report a nonuniform response of different CM field populations to CpGV isolates from CpGV genome groups A to E. Even more strikingly, one field population, NRW-WE, was resistant to all known CpGV genome groups except group B. Single-pair crossing experiments with a susceptible strain, followed by resistance testing of the F 1 offspring, clearly indicated cross-resistance to CpGV isolates that had been considered to be resistance breaking. This finding provides clear evidence of a second, broader type of CpGV resistance with a novel mode of inheritance that cannot be fully explained by Z-linkage of resistance.IMPORTANCE CpGV is registered and used in virtually all commercial apple growing areas worldwide and is therefore the most widely used baculovirus biocontrol agent. Recently, resistance to CpGV products was reported in different countries in Europe, threatening organic growers who rely almost exclusively on CpGV products. This resistance appeared to be targeted against a 24-bp repeat in the pe38 gene in isolate CpGV-M of genome group A, which had been used commercially for many years. On the other hand, resistance could be broken by CpGV isolates from CpGV genome groups B to E. Here, we report clear evidence of a second type of field resistance that is also directed against resistance-breaking isolates of CpGV genome groups C, D, and E and which appears not to be targeted against CpGV pe38. Therefore, we propose to differentiate between type I resistance, which is targeted against pe38 of CpGV genome group A, and a novel type II resistance with an unknown molecular target. This finding stresses the need for further adoption of resistance management strategies for CpGV, since growers cannot rely solely on the use of resistance-breaking CpGV isolates.KEYWORDS baculovirus, biological control, Cydia pomonella, host resistance C ydia pomonella granulovirus (CpGV) (family Baculoviridae) is a double-stranded DNA (dsDNA) virus that is highly virulent to the codling moth (CM), Cydia pomonella L., one of the most destructive insect pests in apple, pear, and walnut orchards. Since CpGV is harmless to nontarget animals and has no detrimental impact on the environment (1, 2), commercial CpGV products became a cornerstone of efficient, highly selective, and environmentally friendly control of CM in integrated and organic pome fruit production (3). Today, CpGV products are registered as biocontrol agents in at least 34 countries worldwide (4).

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“…Resistance to the first strain was overcome, in a practical sense, with a new resistancebreaking variant that had a different resistance mechanism (Eberle et al, 2008;Berling et al, 2009;Graillot et al, 2014). However, very recently, some populations were able to break resistance again and achieve cross resistance to the second strain of CpGV with dominant autosomal inheritance (Sauer et al, 2017a); and a third resistance mechanism has also been identified (Sauer et al, 2017b).…”

Section: Discussionmentioning

confidence: 99%

The role of pathogen diversity on the evolution of resistance in an insect

Li¹

2016

2016 International Congress of Entomology

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My aim is to determine whether baculovirus diversity affects the rate at which resistance evolves. Using Trichoplusia ni as a host, changes in resistance against single versus mixtures of AcMNPV variants were examined in an evolution experiment. AcMNPV variants were isolated using dilution cloning and characterized using RFLP and pathogenicity bioassay. I found that the rate of evolution of resistance to more diverse pathogen infections to be less than that of single variants and the level of resistance was reduced by over 284-fold compared to specific single variants. Identity of the single variants had a major influence on the rate of evolution of resistance. Additionally, I found evidence of higher fitness costs of resistance to more diverse infections. My findings indicate that pathogen diversity should be factored into resistance management strategies for microbial insecticides and provide insight into the role of pathogen diversity on the evolution of resistance to pathogens. .

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Progressive Adaptation of a CpGV Isolate to Codling Moth Populations Resistant to CpGV-M

Cited by 19 publications

References 16 publications

A Third Type of Resistance to Cydia pomonella Granulovirus in Codling Moths Shows a Mixed Z-Linked and Autosomal Inheritance Pattern

A Third Type of Resistance to Cydia pomonella Granulovirus in Codling Moths Shows a Mixed Z-Linked and Autosomal Inheritance Pattern

Evidence for a Second Type of Resistance against Cydia pomonella Granulovirus in Field Populations of Codling Moths

The role of pathogen diversity on the evolution of resistance in an insect

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