A single sex-linked dominant gene does not fully explain the codling moth's resistance to granulovirus

Berling, Marie; Sauphanor, Benoît; Bonhomme, Antoine; Siegwart, Myriam; López‐Ferber, M.

doi:10.1002/ps.3493

Cited by 14 publications

(18 citation statements)

References 41 publications

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“…The current results provide more evidence for autosomal than for Z-linked inheritance. Interestingly, hints of some autosomal properties of CpGV resistance have been also previously reported for German and French CM populations (25,32), although these findings have not yet been replicated.…”

Section: Discussionmentioning

confidence: 83%

“…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%

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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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Section: Discussionmentioning

confidence: 83%

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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“…For the codling moth strain CpR, which originated from a resistant field population in south Germany, as well as the genetically homogenous laboratory strain CpRR1, which derived from CpR, the mode of inheritance was revealed to be incompletely dominant, monogenic, and linked to the Z (sex) chromosome (15,16). A similar mode of inheritance was also observed in resistant Czech and French codling moth populations arguing for a more or less universal mode of resistance in Europe (17,18). These data led to the hypothesis that a genetic adaptation of codling moth to CpGV-M infection had occurred and was selected for by the intensive use of products containing CpGV-M (15).…”

mentioning

confidence: 70%

“…The preponderant occurrence of resistance of codling moth to the virus isolate CpGV-M in organic apple plantations, where the application of CpGV products was the main and often only measure to control codling moth, is no doubt the result of mutation and selection, the guiding principle of Darwinian evolution in insect populations (15,29,30). Studies showing that naturally occurring geographic CpGV isolates, such as I12, NPP-R1/R4, and others, were still infectious to resistant codling moth populations and led to the development and registration of improved resistancebreaking CpGV products (18,(30)(31)(32). Consequently, the understanding of resistance to CpGV and resistance-breaking by CpGV are of particular importance for codling moth control and may serve as a model for other baculoviruses used in insect pest control.…”

Section: Discussionmentioning

confidence: 99%

Baculovirus resistance in codling moth is virus isolate-dependent and the consequence of a mutation in viral genepe38

Gebhardt

Eberle

Radtke

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

103

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Significance Registered in 34 countries worldwide, Cydia pomonella granulovirus (CpGV) is a highly important biological agent to control the codling moth in pome fruit production. Since 2005, 38 codling moth field populations resistant to CpGV products containing the Mexican isolate (CpGV-M) were discovered in Europe, and this was the first demonstrated field resistance against commercial baculovirus products. By identifying and sequencing different resistance-breaking CpGV isolates, it was found that resistance of codling moth is directed toward CpGV-M only. As shown by mutation experiments, CpGV-M is prone to resistance because of a 24-nucleotide repeat within the viral gene pe38 . Thus, pe38 can be used as a genetic marker to identify resistance-breaking CpGV isolates for resistance management programs.

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“…In the armyworm Spodoptera frugiperda , a fivefold difference in the susceptibility of two laboratory colonies to three different baculoviruses has been attributed to a single or few autosomal genes (Reichelderfer and Benton, 1974). In contrast, in the codling moth, this susceptibility appears to be under multigenic control (Berling et al, 2013). Maintaining the differences in susceptibility between insect populations does not seem to rely on the presence of the virus.…”

Section: Resistance To Biocontrol Agentsmentioning

confidence: 99%

Resistance to bio-insecticides or how to enhance their sustainability: a review

Siegwart

Graillot

Lopez³

et al. 2015

Front. Plant Sci.

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149

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After more than 70 years of chemical pesticide use, modern agriculture is increasingly using biological control products. Resistances to conventional insecticides are wide spread, while those to bio-insecticides have raised less attention, and resistance management is frequently neglected. However, a good knowledge of the limitations of a new technique often provides greater sustainability. In this review, we compile cases of resistance to widely used bio-insecticides and describe the associated resistance mechanisms. This overview shows that all widely used bio-insecticides ultimately select resistant individuals. For example, at least 27 species of insects have been described as resistant to Bacillus thuringiensis toxins. The resistance mechanisms are at least as diverse as those that are involved in resistance to chemical insecticides, some of them being common to bio-insecticides and chemical insecticides. This analysis highlights the specific properties of bio-insecticides that the scientific community should use to provide a better sustainability of these products.

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A single sex-linked dominant gene does not fully explain the codling moth's resistance to granulovirus

Abstract: Transmission of granulovirus resistance in the RGV-8 strain of C. pomonella cannot be fully explained by the effect of a locus located on the Z chromosome. The action of other factors needs to be considered.

Cited by 14 publications

References 41 publications

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

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

Baculovirus resistance in codling moth is virus isolate-dependent and the consequence of a mutation in viral genepe38

Resistance to bio-insecticides or how to enhance their sustainability: a review

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