Rapid Emergence of Baculovirus Resistance in Codling Moth Due to Dominant, Sex-Linked Inheritance

Asser-Kaiser, S.; Fritsch, Eva; Undorf-Spahn, Karin; Kienzle, Jörg; Eberle, Karolin E.; Gund, Nadine A.; Reineke, Annette; Zebitz, C. P. W.; Heckel, David G.; Huber, Jürg; Jehle, Johannes A.

doi:10.1126/science.1146542

Cited by 132 publications

(209 citation statements)

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“…It is conceivable that these types have slightly different biological activities and contribute to the virulence of the different isolates. Indeed, it was recently found that I12 is able to infect C. pomonella strains that were shown to be resistant to CpGV-M (Eberle et al, 2008;Asser-Kaiser et al, 2007). Our analyses further propose an increase in virulence of type A and D CpGVs against C. pomonella, compared with the more ancestral type C seen during CpGV evolution.…”

Section: Discussionsupporting

confidence: 56%

Diversity and evolution of the Cydia pomonella granulovirus

Eberle

Sayed

Rezapanah³

et al. 2009

Journal of General Virology

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Eight new field isolates of Cydia pomonella granulovirus (CpGV) originating in Iran and Georgia and one English CpGV isolate were analysed for restriction fragment length polymorphisms (RFLPs) and by partial genome amplification and sequencing. According to the observed RFLPs, most of the predominant genotypes of these isolates could be assigned to those present in previously found isolates originating from Mexico (CpGV-M), England (CpGV-E) and Russia (CpGV-R). We suggest that these isolates should be designated genome A, B and C types, respectively. A fourth genome type was identified in three isolates and is designated D type. The isolates with A, B and D type genomes contained four open reading frames (ORFs) (ORF63-ORF66) not present in C type genomes. The lack of these ORFs in other granuloviruses suggests that the C type genome is evolutionarily ancestral to the other genome types. The B and D type genomes contained an additional insertion of a non-protein coding region of 0.7 kb, which was at different genome locations. Analysis of the partial gene sequences of late expression factor 8 (lef-8), lef-9 and polyhedrin/granulin (polh/gran) genes revealed single nucleotide polymorphisms (SNPs) that corresponded to the RFLP types. Phylogenetic analyses based on these SNPs corroborated the proposed ancestry of the C type genome. C type viruses were also less virulent to neonate codling moth larvae than the other virus types. In conclusion, the known diversity of CpGV isolates can be described by four major genome types, which appear to exist in different isolates as genotype mixtures.

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Section: Discussionsupporting

confidence: 56%

Diversity and evolution of the Cydia pomonella granulovirus

Eberle

Sayed

Rezapanah³

et al. 2009

Journal of General Virology

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“…Resistance was confirmed for several C. pomonella populations collected in organic orchards where CpGV treatments had failed (3,30). This resistance to CpGV is the first case of resistance to a virus observed in field populations of an insect.…”

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confidence: 93%

Cydia pomonella granulovirus Genotypes Overcome Virus Resistance in the Codling Moth and Improve Virus Efficiency by Selection against Resistant Hosts

Berling¹,

Blachère-López²,

Soubabère

et al. 2009

Appl Environ Microbiol

109

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Cydia pomonella granulovirus (CpGV) has been used for 15 years as a bioinsecticide in codling moth (Cydia pomonella) control. In 2004, some insect populations with low susceptibility to the virus were detected for the first time in southeast France. RGV, a laboratory colony of codling moths resistant to the CpGV-M isolate used in the field, was established with collection of resistant insects in the field followed by an introgression of the resistant trait into a susceptible colony (Sv). The resistance level (based on the 50% lethal concentrations [LC 50 s]) of the RGV colony to the CpGV-M isolate, the active ingredient in all commercial virus formulations in Europe, appeared to be over 60,000-fold compared to the Sv colony. The efficiency of CpGV isolates from various other regions was tested on RGV. Among them, two isolates (I12 and NPP-R1) presented an increased pathogenicity on RGV. I12 had already been identified as effective against a resistant C. pomonella colony in Germany and was observed to partially overcome the resistance in the RGV colony. The recently identified isolate NPP-R1 showed an even higher pathogenicity on RGV than other isolates, with an LC 50 of 166 occlusion bodies (OBs)/l, compared to 1.36 ؋ 10 6 OBs/l for CpGV-M. Genetic characterization showed that NPP-R1 is a mixture of at least two genotypes, one of which is similar to CpGV-M. The 2016-r4 isolate obtained from four successive passages of NPP-R1 in RGV larvae had a sharply reduced proportion of the CpGV-M-like genotype and an increased pathogenicity against insects from the RGV colony.

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“…CpGV resistance was characterized in detail for the CM strain CpRR1, a genetically homogenous inbred strain that derived from a resistant CM field population in southern Germany (13). For CpRR1, systemic resistance in all instars was observed, and an early block in virus replication was found to be inherited in an incompletely dominant monogenic mode linked to the Z chromosome (13,19,20).…”

mentioning

confidence: 99%

“…From 2005 on, however, the emergence of field resistance of CM populations against CpGV products was detected in Germany and France (11,12). Meanwhile, CpGVresistant CM populations have been documented in 38 orchards, mainly organic apple orchards from different European countries, including Germany (22 orchards), France (3 orchards), Switzerland (22 orchards), Italy (6 orchards), Austria (2 orchards), The Netherlands (2 orchards), and the Czech Republic (1 orchard) (13)(14)(15)(16)(17). Some of these field populations were 1,000 to 100,000 times less susceptible to CpGV-M than were typical susceptible larvae (13).…”

mentioning

confidence: 99%

“…Meanwhile, CpGVresistant CM populations have been documented in 38 orchards, mainly organic apple orchards from different European countries, including Germany (22 orchards), France (3 orchards), Switzerland (22 orchards), Italy (6 orchards), Austria (2 orchards), The Netherlands (2 orchards), and the Czech Republic (1 orchard) (13)(14)(15)(16)(17). Some of these field populations were 1,000 to 100,000 times less susceptible to CpGV-M than were typical susceptible larvae (13). When 33 resistant and nonresistant CM populations from different geographic origins were analyzed by using microsatellite (simple sequence repeats [SSR]) and mitochondrial DNA markers, it was found that these populations did not differ significantly from each other, and genetic differentiation between resistant and nonresistant populations was not possible (18).…”

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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Rapid Emergence of Baculovirus Resistance in Codling Moth Due to Dominant, Sex-Linked Inheritance

Cited by 132 publications

References 5 publications

Diversity and evolution of the Cydia pomonella granulovirus

Diversity and evolution of the Cydia pomonella granulovirus

Cydia pomonella granulovirus Genotypes Overcome Virus Resistance in the Codling Moth and Improve Virus Efficiency by Selection against Resistant Hosts

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

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