High stability and no fitness costs of the resistance of codling moth to Cydia pomonella granulovirus (CpGV-M)

The complete genome of an endemic South African Cydia pomonella granulovirus isolate was sequenced and analyzed. Several missing or truncated open reading frames (ORFs) were identified, including a 24 bp deletion in the pe38 gene which is reported to be associated with type I resistance-breaking potential. Comparison of single nucleotide polymorphisms (SNPs) with five other fully sequenced CpGV isolates identified 67 unique events, 47 of which occurred within ORFs, leading to several amino acid changes. Further analysis of single nucleotide variations (SNVs) within CpGV-SA revealed that this isolate consists of mixed genotypes. Phylogenetic analysis using complete genome sequences placed CpGV-SA basal to M, I12 and E2 and distal to S and I07 but with no distinct classification into any of the previously defined CpGV genogroups. These results suggest that CpGV-SA is a novel and genetically distinct isolate with significant potential as a biopesticide for management of codling moth (CM), not only in South Africa, but potentially in other pome fruit producing countries, particularly where CM resistance to CpGV has been reported.

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Importance of the Host Phenotype on the Preservation of the Genetic Diversity in Codling Moth Granulovirus

Viruses ◽

10.3390/v11070621 ◽

2019 ◽

Vol 11 (7) ◽

pp. 621 ◽

Cited By ~ 2

Author(s):

Graillot ◽

Blachere-López ◽

Besse ◽

Siegwart ◽

López-Ferber

Keyword(s):

Genetic Diversity ◽

Cydia Pomonella ◽

Codling Moth ◽

Type I ◽

Host Genotype ◽

Host Colony ◽

Type I Resistance ◽

Cydia Pomonella Granulovirus ◽

Marker Virus ◽

Mexican Isolate

To test the importance of the host genotype in maintaining virus genetic diversity, five experimental populations were constructed by mixing two Cydia pomonella granulovirus isolates, the Mexican isolate CpGV-M and the CpGV-R5, in ratios of 99% M + 1% R, 95% M + 5% R, 90% M + 10% R, 50% M + 50% R, and 10% M + 90% R. CpGV-M and CpGV-R5 differ in their ability to replicate in codling moth larvae carrying the type I resistance. This ability is associated with a genetic marker located in the virus pe38 gene. Six successive cycles of replication were carried out with each virus population on a fully-permissive codling moth colony (CpNPP), as well as on a host colony (RGV) that carries the type I resistance, and thus blocks CpGV-M replication. The infectivity of offspring viruses was tested on both hosts. Replication on the CpNPP leads to virus lineages preserving the pe38 markers characteristic of both isolates, while replication on the RGV colony drastically reduces the frequency of the CpGV-M pe38 marker. Virus progeny obtained after replication on CpNPP show consistently higher pathogenicity than that of progeny viruses obtained by replication on RGV, independently of the host used for testing.

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Cross-Resistance of the Codling Moth against Different Isolates of Cydia pomonella Granulovirus Is Caused by Two Different but Genetically Linked Resistance Mechanisms

Viruses ◽

10.3390/v13101952 ◽

2021 ◽

Vol 13 (10) ◽

pp. 1952

Author(s):

Annette J. Sauer ◽

Eva Fritsch ◽

Karin Undorf-Spahn ◽

Kento Iwata ◽

Regina G. Kleespies ◽

...

Keyword(s):

Biological Control Agent ◽

Cydia Pomonella ◽

Codling Moth ◽

Resistance Mechanisms ◽

Cross Resistance ◽

Viral Gene ◽

Type I ◽

Type Ii ◽

Cydia Pomonella Granulovirus ◽

Type Ii Resistance

Cydia pomonella granulovirus (CpGV) is a widely used biological control agent of the codling moth. Recently, however, the codling moth has developed different types of field resistance against CpGV isolates. Whereas type I resistance is Z chromosomal inherited and targeted at the viral gene pe38 of isolate CpGV-M, type II resistance is autosomal inherited and targeted against isolates CpGV-M and CpGV-S. Here, we report that mixtures of CpGV-M and CpGV-S fail to break type II resistance and is expressed at all larval stages. Budded virus (BV) injection experiments circumventing initial midgut infection provided evidence that resistance against CpGV-S is midgut-related, though fluorescence dequenching assay using rhodamine-18 labeled occlusion derived viruses (ODV) could not fully elucidate whether the receptor binding or an intracellular midgut factor is involved. From our peroral and intra-hemocoel infection experiments, we conclude that two different (but genetically linked) resistance mechanisms are responsible for type II resistance in the codling moth: resistance against CpGV-M is systemic whereas a second and/or additional resistance mechanism against CpGV-S is located in the midgut of CpR5M larvae.

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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 ◽

10.1080/095831500750016424 ◽

2000 ◽

Vol 10 (5) ◽

pp. 627-640 ◽

Cited By ~ 26

Author(s):

J. Ballard ◽

D. J. Ellis ◽

C. C. Payne

Keyword(s):

Field Experiments ◽

Cydia Pomonella ◽

Codling Moth ◽

Cydia Pomonella Granulovirus

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

Applied and Environmental Microbiology ◽

10.1128/aem.01998-08 ◽

2008 ◽

Vol 75 (4) ◽

pp. 925-930 ◽

Cited By ~ 62

Author(s):

Marie Berling ◽

Christine Blachere-Lopez ◽

Olivier Soubabere ◽

Xavier Lery ◽

Antoine Bonhomme ◽

...

Keyword(s):

Genetic Characterization ◽

Cydia Pomonella ◽

Codling Moth ◽

Resistance Level ◽

Laboratory Colony ◽

Occlusion Bodies ◽

Insect Populations ◽

Cydia Pomonella Granulovirus ◽

First Time ◽

Resistant Trait

ABSTRACT 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 [LC50s]) 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 LC50 of 166 occlusion bodies (OBs)/μl, compared to 1.36 ï¿½ 106 OBs/μl 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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Partial Loss of Inheritable Type I Resistance of Codling Moth to Cydia pomonella granulovirus

Viruses ◽

10.3390/v11060570 ◽

2019 ◽

Vol 11 (6) ◽

pp. 570 ◽

Cited By ~ 1

Author(s):

Jiangbin Fan ◽

Jörg Wennmann ◽

Johannes Jehle

Keyword(s):

Current Knowledge ◽

Full Range ◽

Cydia Pomonella ◽

Codling Moth ◽

Single Pair ◽

Type I ◽

Partial Loss ◽

Resistance Level ◽

Type I Resistance ◽

Cydia Pomonella Granulovirus

Current knowledge of the field resistance of codling moth (CM, Cydia pomonella, L) against Cydia pomonella granulovirus (CpGV) is based mainly on the interaction between the Mexican isolate CpGV-M and CpRR1, a genetically homogeneous CM inbreed line carrying type I resistance. The resistance level of laboratory-reared CpRR1 to CpGV-M was recently found to have decreased considerably, compared to the initially high resistance. To understand the background of this phenomenon, CpRR1 larvae were exposed over several generations to CpGV-M for re-selection of the original resistance level. After five and seven generations of selection, new CpRR1_F5 and CpRR1_F7 lines were established. The resistance ratio of these selected lines was determined by full range bioassays. The CpRR1_F5 strain regained a higher level of resistance against CpGV up to 104-fold based on LC50 values compared to susceptible larvae (CpS), which indicated that the absence of virus selection had resulted in a reduction of resistance under laboratory rearing conditions. In addition, some fitness costs of fecundity were observed in CpRR1_F5. Single-pair crossings between CpRR1_F5 or CpRR1_F7 with susceptible CpS moths revealed a dominant but not fully sex-linked inheritance, which suggests a partial loss of previous resistance traits in CpRR1.

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Transcriptome of Cydia pomonella granulovirus in susceptible and type I resistant codling moth larvae

Journal of General Virology ◽

10.1099/jgv.0.001566 ◽

2021 ◽

Vol 102 (3) ◽

Cited By ~ 1

Author(s):

Jörg T. Wennmann ◽

Diana Pietruska ◽

Johannes A. Jehle

Keyword(s):

Gene Expression ◽

Fat Body ◽

Cydia Pomonella ◽

Codling Moth ◽

Viral Gene ◽

Type I ◽

Pome Fruit ◽

Type I Resistance ◽

Cydia Pomonella Granulovirus

The baculovirus Cydia pomonella granulovirus (CpGV) is a biocontrol agent used worldwide against the codling moth (CM), Cydia pomonella L., a severe pest in organic and integrated pome fruit production. Its successful application is increasingly challenged by the occurrence of CM populations resistant to commercial CpGV products. Whereas three types (I–III) of CpGV resistance have been identified, type I resistance compromising the efficacy of CpGV-M, the so-called Mexican isolate of CpGV, is assumed to be the most widely distributed resistance type in Central Europe. Despite the wide use of CpGV products as biocontrol agents, little information is available on gene-expression levels in CM larvae. In this study, the in vivo transcriptome of CpGV-M infecting susceptible (CpS) and resistant (CpRR1) CM larvae was analysed at 24, 48, 72, 96 and 120 hours post infection in the midgut and fat body tissue by using a newly developed microarray covering all ORFs of the CpGV genome. According to their transcript abundance, the CpGV genes were grouped into four temporal clusters to which groups of known and unknown function could be assigned. In addition, sets of genes differentially expressed in the midgut and fat body were found in infected susceptible CpS larvae. For the resistant CpRR1 larvae treated with CpGV-M, viral entry in midgut cells could be confirmed from onset but a significantly reduced gene expression, indicating that type I resistance is associated with a block of viral gene transcription and replication.

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Overcoming the resistance of codling moth against conventional Cydia pomonella granulovirus (CpGV-M) by a new isolate CpGV-I12

Journal of Invertebrate Pathology ◽

10.1016/j.jip.2008.03.003 ◽

2008 ◽

Vol 98 (3) ◽

pp. 293-298 ◽

Cited By ~ 55

Author(s):

K.E. Eberle ◽

S. Asser-Kaiser ◽

S.M. Sayed ◽

H.T. Nguyen ◽

J.A. Jehle

Keyword(s):

Cydia Pomonella ◽

Codling Moth ◽

Cydia Pomonella Granulovirus

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Cryptophlebia peltastica Nucleopolyhedrovirus Is Highly Infectious to Codling Moth Larvae and Cells

Applied and Environmental Microbiology ◽

10.1128/aem.00795-19 ◽

2019 ◽

Vol 85 (17) ◽

Author(s):

Jörg T. Wennmann ◽

Marina Eigenbrod ◽

Tamryn Marsberg ◽

Sean D. Moore ◽

Caroline M. Knox ◽

...

Keyword(s):

High Speed ◽

Cydia Pomonella ◽

Economic Value ◽

Codling Moth ◽

Fruit Production ◽

Laboratory Culture ◽

Pome Fruit ◽

Content Type ◽

Imminent Threat ◽

Cydia Pomonella Granulovirus

ABSTRACT Cydia pomonella granulovirus (CpGV) is a cornerstone of codling moth (Cydia pomonella) control in integrated and organic pome fruit production, though different types of resistance to CpGV products have been recorded in codling moth field populations in Europe for several years. Recently, a novel baculovirus named Cryptophlebia peltastica nucleopolyhedrovirus (CrpeNPV) was isolated from a laboratory culture of the litchi moth, Cryptophlebia peltastica, in South Africa. Along with CpGV, it is the third known baculovirus that is infectious to codling moth. In the present study, parameters of infectiveness of CrpeNPV, such as the median lethal concentration and median survival time, were determined for codling moth larvae susceptible or resistant to CpGV. In addition, the permissiveness of a codling moth cell line with respect to infection by CrpeNPV budded virus was demonstrated by infection and gene expression studies designed to investigate the complete replication cycle. Investigations of the high degree of virulence of CrpeNPV for codling moth larvae and cells are of high significant scientific and economic value and may offer new strategies for the biological control of susceptible and resistant populations of codling moth. IMPORTANCE The emergence of codling moth populations resistant to commercially applied isolates of CpGV is posing an imminent threat to organic pome fruit production. Very few CpGV isolates are left that are able to overcome the reported types of resistance, emphasizing the demand for new and highly virulent baculoviruses. Here we report the recently discovered CrpeNPV as highly infectious to all types of resistant codling moth populations with a high speed of killing, making it a promising candidate baculovirus in fighting the spread of resistant codling moth populations.

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