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

Abstract

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).

Novel resistance to Cydia pomonella granulovirus (CpGV) in codling moth shows autosomal and dominant inheritance and confers cross-resistance to different CpGV genome groups

“…These findings clearly explain the previous experimental observations questioning a Z-linked inheritance in NRW-WE [24]. Therefore, it corroborates the previous prediction of a second type (II) of resistance, present in NRW-WE and consequently in CpR5M and CpR5S, which is different from type I resistance in CpRR1.…”

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

“…This was the first time that resistance of insect populations to commercial baculovirus products had been reported. In the following years, field resistance of C. pomonella populations to CpGV products was observed in about 40 apple plantations in Austria, the Czech Republic, France, Germany, Italy, the Netherlands, and Switzerland (10)(11)(12)(13). Acquired resistance of insects to baculoviruses has been described also for several insect-baculovirus associations, such as Phthorimaea operculella-Phthorimaea operculella granulovirus (PhopGV) (14), Anticarsia gemmatalis-Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV) (15), Trichoplusia ni-Trichoplusia ni single nucleopolyhedrovirus (TnSNPV) (16,17), and Adoxophyes honmai-Adoxophyes honmai nucleopolyhedrovirus (AdhoNPV) (18,19).…”

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

“…After decades of successful application of CpGV-M, the biological control of C. pomonella became hampered by the occurrence of field resistance against CpGV-M, which was reported to have been detected since 2005 (11,12). Resistant populations of C. pomonella were reported from organic apple orchards in Austria, Czech Republic, France, Germany, Italy, Netherlands, and Switzerland and were characterized by a 1,000-fold-to 100,000-fold-reduced range of susceptibilities to CpGV-M, preventing economic control of C. pomonella and posing a serious threat to organic apple production (11). At least three different types of CpGV resistances have been identified.…”

“…At least three different types of CpGV resistances have been identified. Type I resistance is targeted against isolate CpGV-M with a sex-linked inheritance located on the Z chromosome (11). A genetically homogeneous laboratory C. pomonella strain carrying this type of resistance was established and named CpRR1 (8).…”

“…A second type of resistance (type II) was identified in a genetically homogenous laboratory strain called CpR5M, which derived from a resistant C. pomonella field population in Northwest Germany (11). Larvae of CpR5M exhibited resistance to CpGV-M and also to CpGV-S, CpGV-I12, and CpGV-I07.…”