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.
WennmannJT,
RadtkeP,
EberleKE,
Gueli AllettiG,
JehleJA.
Deciphering single nucleotide polymorphisms and evolutionary trends in isolates of the Cydia pomonella granulovirus. Viruses2017; 9:227 [View Article][PubMed]
LaceyLA,
Shapiro-IlanDI.
Microbial control of insect pests in temperate orchard systems: potential for incorporation into IPM. Annu Rev Entomol2008; 53:121–144 [View Article][PubMed]
GrönerA.
Specificity and safety of baculoviruses. In
GranadosRR,
FedericiBA.
(editors) The Biology of Baculoviruses1 Boca Raton, Florida: CRC Press; 1986 pp 177–202
HuberJ.
Western Europe. In
Hunter-FujitaFR,
EntwistlePF,
EvansHF,
CrookNE.
(editors) Insect Viruses and Pest Management New York: Wiley; 1998 pp 201–215
FanJ,
WennmannJT,
WangD,
JehleJA.
Novel diversity and virulence patterns found in new isolates of Cydia pomonella granulovirus from China. Appl Environ Microbiol2019; 86:e02000-19
ArneodoJD,
De AnnaJ,
SalvadorR,
FarinonM,
QuintanaG.
Prospection and molecular analysis of CpGV isolates infecting Cydia pomonella at different geographical locations in Argentina. Ann Appl Biol2015; 166:67–74
GanE,
LiX,
YuH,
WuZ,
LiX.
Virulence determination for three native Cydia pomonella granulovirus strains and their control effect in field. J Northwest A&F Univ2011; 39:119–122
RezapanahM,
Shojai-EstabraghS,
HuberJ,
JehleJA.
Molecular and biological characterization of new isolates of Cydia pomonella granulovirus from Iran. J Pest Sci2008; 81:187–191
CrookNE,
SpencerRA,
PayneCC,
LeisyDJ.
Variation in Cydia pomonella granulosis virus isolates and physical maps of the DNA from three variants. J Gen Virol1985; 66:2423–2430
FanJ,
JehleJA,
WennmannJT.
Population structure of Cydia pomonella granulovirus isolates revealed by quantitative analysis of genetic variation. Virus Evol2020; 6:veaa073
WennmannJT,
FanJ,
JehleJA.
Bacsnp: using single nucleotide polymorphism (SNP) specificities and frequencies to identify genotype composition in baculoviruses. Viruses2020; 12:625 [View Article][PubMed]
GraillotB,
BayleS,
Blachere-LopezC,
BesseS,
SiegwartM et al. Biological characteristics of experimental genotype mixtures of Cydia pomonella granulovirus (CpGV): Ability to control susceptible and resistant pest populations. Viruses2016; 8:147 [View Article][PubMed]
AllettiGG,
SauerAJ,
WeihrauchB,
FritschE,
Undorf-SpahnK et al. Using next generation sequencing to identify and quantify the genetic composition of resistance-breaking commercial isolates of Cydia pomonella granulovirus. Viruses2017; 9:250 [View Article][PubMed]
ZinggD,
ZügerM,
BollhalderF,
AndermattM.
Use of resistance overcoming CpGV isolates and CpGV resistance situation of the codling moth in Europe seven years after the first discovery of resistance to CpGV-M. IOBC-WPRS Bulletin2011; 66:401–404
FritschE,
Undorf-SpahnK,
KienzleJ,
ZebitzCPW,
HuberJ.
Apfelwickler-Granulovirus: Erste Hinweise auf Unterschiede in Der Empfindlichkeit lokaler Apfelwickler-Populationen. Nachrichtenbl Deut Pflanzenschutzd2005; 57:29–34
SchmittA,
BisuttiIL,
LadurnerE,
BenuzziM,
SauphanorB.
The occurrence and distribution of resistance of codling moth to Cydia pomonella granulovirus in Europe. J Appl Entomol2013; 137:641–649
ZichováT,
FaltaV,
KocourekF,
StaráJ.
Differences in the susceptibility of codling moth populations to Cydia pomonella granulovirus in the Czech Republic. Hort Sci2011; 38:21–26
Asser-KaiserS,
HeckelDG,
JehleJA.
Sex linkage of CpGV resistance in a heterogeneous field strain of the codling moth Cydia pomonella (L.). J Invertebr Pathol2010; 103:59–64 [View Article][PubMed]
BerlingM,
Blachere-LopezC,
SoubabereO,
LeryX,
BonhommeA et al.Cydia pomonella granulovirus genotypes overcome virus resistance in the codling moth and improve virus efficiency by selection against resistant hosts. Appl Environ Microbiol2009; 75:925–930 [View Article][PubMed]
Asser-KaiserS,
FritschE,
Undorf-SpahnK,
KienzleJ,
EberleKE et al. Rapid emergence of baculovirus resistance in codling moth due to dominant, sex-linked inheritance. Science2007; 317:1916–1918 [View Article][PubMed]
JehleJA,
Schulze-BoppS,
Undorf-SpahnK,
FritschE.
Evidence for a second type of resistance against Cydia pomonella Granulovirus in field populations of codling moths. Appl Environ Microbiol2017; 83:e02330–16 [View Article][PubMed]
SauerAJ,
FritschE,
Undorf-SpahnK,
NguyenP,
MarecF et al. Novel resistance to Cydia pomonella granulovirus (CpGV) in codling moth shows autosomal and dominant inheritance and confers cross-resistance to different CpGV genome groups. PLoS One2017; 12:e0179157 [View Article][PubMed]
SauerAJ,
Schulze-BoppS,
FritschE,
Undorf-SpahnK,
JehleJA.
A third type of resistance to Cydia pomonella granulovirus in codling moths shows a mixed Z-linked and autosomal inheritance pattern. Appl and Environ Microbiol2017; 83:e01036–17
GebhardtMM,
EberleKE,
RadtkeP,
JehleJA.
Baculovirus resistance in codling moth is virus isolate-dependent and the consequence of a mutation in viral gene pe38. Proc Natl Acad Sci U S A2014; 111:15711–15716 [View Article][PubMed]
Asser-KaiserS,
RadtkeP,
El-SalamounyS,
WinstanleyD,
JehleJA.
Baculovirus resistance in codling moth (Cydia pomonella L.) caused by early block of virus replication. Virology2011; 410:360–367
ShresthaA,
BaoK,
ChenY-R,
ChenW,
WangP et al. Global analysis of baculovirus Autographa californica multiple nucleopolyhedrovirus gene expression in the midgut of the Lepidopteran host Trichoplusia ni
. J Virol2018; 92:e01277–18 [View Article][PubMed]
ChenY-R,
ZhongS,
FeiZ,
HashimotoY,
XiangJZ et al. The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol2013; 87:6391–6405 [View Article][PubMed]
Ivaldi-SenderC.
Techniques simple pour l’élévage permanent de la tordeuse orientale, Grapholita molesta (Lep., Tortricidae), sur milieu artificiel. Ann Zool Ecol Anim1974; 6:337–343
JehleJA,
BackhausH,
FritschE,
HuberJ.
Physical map of the Cryptophlebia leucotreta granulosis virus genome and its relationship to the genome of Cydia pomonella granulosis virus. J Gen Virol1992; 73:1621–1626 [View Article][PubMed]
LuqueT,
FinchR,
CrookN,
O'ReillyDR,
WinstanleyD.
The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol2001; 82:2531–2547 [View Article][PubMed]
XuB,
YooS,
GuarinoLA.
Differential transcription of baculovirus late and very late promoters: fractionation of nuclear extracts by phosphocellulose chromatography. J Virol1995; 69:2912–2917 [View Article][PubMed]
WanF,
YinC,
TangR,
ChenM,
WuQ et al. A chromosome-level genome assembly of Cydia pomonella provides insights into chemical ecology and insecticide resistance. Nat Commun2019; 10:4237 [View Article][PubMed]
KovacsGR.
Novel regulatory properties of the IEl and IEO transactivators encoded by the baculovirus Autographa californica multicapsid nuclear polyhedrosis virus. J Virol1991; 65:8
ThiemSM,
MillerLK.
Identification, sequence, and transcriptional mapping of the major capsid protein gene of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol1989; 63:2008–2018 [View Article][PubMed]
LungO,
WestenbergM,
VlakJM,
ZuidemaD,
BlissardGW.
Pseudotyping Autographa californica multicapsid nucleopolyhedrovirus (AcMNPV): F proteins from group II NPVs are functionally analogous to AcMNPV gp64. J Virol2002; 76:5729–5736 [View Article][PubMed]
EberleKE,
Asser-KaiserS,
SayedSM,
NguyenHT,
JehleJA.
Overcoming the resistance of codling moth against conventional Cydia pomonella granulovirus (CpGV-M) by a new isolate CpGV-I12. J Invertebr Pathol2008; 98:293–298 [View Article][PubMed]
YamagishiJ,
BurnettED,
HarwoodSH,
BlissardGW.
The AcMNPV pp31 gene is not essential for productive AcMNPV replication or late gene transcription but appears to increase levels of most viral transcripts. Virology2007; 365:34–47 [View Article][PubMed]