Asymmetrical cross-resistance between<i>Bacillus thuringiensis</i>toxins Cry1Ac and Cry2Ab in pink bollworm

Tabashnik, Bruce E.; Unnithan, Gopalan C.; Masson, Luke; Crowder, David W.; Li, Xianchun; Carrière, Yves

doi:10.1073/pnas.0901351106

Cited by 115 publications

(115 citation statements)

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“…The first kind of pleiotropic effect can be named cross-infectivity by analogy to cross-resistance of microbes, insects, or weeds to different (bio)chemical compounds in a medical or agricultural context (35)(36)(37)(38)(39). It can be defined as the effect of a single mutational event which leads to the breakdown of at least two plant resistance genes or alleles, an initial one, which exerts selection pressure on the pathogen population leading to the fixation of an RB mutation, and a second one, which does not play any role in the fixation of the RB mutation.…”

Section: Discussionmentioning

confidence: 99%

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

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The structural pattern of infectivity matrices, which contains infection data resulting from inoculations of a set of hosts by a set of parasites, is a key parameter for our understanding of biological interactions and their evolution. This pattern determines the evolution of parasite pathogenicity and host resistance, the spatiotemporal distribution of host and parasite genotypes, and the efficiency of disease control strategies. Two major patterns have been proposed for plant-virus genotype infectivity matrices. In the gene-for-gene model, infectivity matrices show a nested pattern, where the host ranges of specialist virus genotypes are subsets of the host ranges of less specialized viruses. In contrast, in the matching-allele (MA) model, each virus genotype is specialized to infect one (or a small set of) host genotype(s). The corresponding infectivity matrix shows a modular pattern where infection is frequent for plants and viruses belonging to the same module but rare for those belonging to different modules. We analyzed the structure of infectivity matrices between Potato virus Y (PVY) and plant genotypes in the family Solanaceae carrying different eukaryotic initiation factor 4E (eIF4E)-coding alleles conferring recessive resistance. Whereas this system corresponds mechanistically to an MA model, the expected modular pattern was rejected based on our experimental data. This was mostly because PVY mutations involved in adaptation to a particular plant genotype displayed frequent pleiotropic effects, conferring simultaneously an adaptation to additional plant genotypes with different eIF4E alleles. Such effects should be taken into account for the design of strategies of sustainable control of PVY through plant varietal mixtures or rotations. IMPORTANCEThe interaction pattern between host and virus genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. We found that the structure of the interaction between Potato virus Y (PVY) variants and host plants in the family Solanaceae departs significantly from the current model of interaction considered for these organisms because of frequent pleiotropic effects of virus mutations. These mutational effects allow the virus to expand rapidly its range of host plant genotypes, make it very difficult to predict the effects of mutations in PVY infectivity factors, and raise concerns about strategies of sustainable management of plant genetic resistance to viruses. T he interaction pattern between host and parasite genotypes has important consequences on their respective evolution and on issues regarding the application of disease control strategies. This pattern determines to a large extent the maintenance of genetic diversity in host and parasite populations (1), the structure of these populations in space and time (2, 3), and the evolution of parasite pathogenicity and host resistance (4).Different models of host-parasite interaction and coevolution have been proposed (3, 5) (F...

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Section: Discussionmentioning

confidence: 99%

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Moury¹,

Janzac

Ruellan³

et al. 2014

J Virol

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“…The gene pyramiding strategy to combine Cry1Ac and Cry2Ab has proven to be effective in delaying the development of insect resistance to Bt toxins (25,26). Nonetheless, resistance to Cry2Ab has been reported in Heliothis virescens, Helicoverpa zea, Helicoverpa armigera, Helicoverpa punctigera, Pectinophora gossypiella, and Trichoplusia ni (8,(27)(28)(29)(30)(31)(32). These reports have indicated that Cry2Ab-resistant alleles are present in insect populations, and the frequency of resistant alleles will increase with selection.…”

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confidence: 91%

Resistance to Bacillus thuringiensis Toxin Cry2Ab in Trichoplusia ni Is Conferred by a Novel Genetic Mechanism

Song

Kain

Cassidy

et al. 2015

Appl Environ Microbiol

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The resistance to the Bacillus thuringiensis (Bt) toxin Cry2Ab in a greenhouse-originated Trichoplusia ni strain resistant to both Bt toxins Cry1Ac and Cry2Ab was characterized. Biological assays determined that the Cry2Ab resistance in the T. ni strain was a monogenic recessive trait independent of Cry1Ac resistance, and there existed no significant cross-resistance between Cry1Ac and Cry2Ab in T. ni. From the dual-toxin-resistant T. ni strain, a strain resistant to Cry2Ab only was isolated, and the Cry2Ab resistance trait was introgressed into a susceptible laboratory strain to facilitate comparative analysis of the Cry2Ab resistance with the susceptible T. ni strain. Results from biochemical analysis showed no significant difference between the Cry2Ab-resistant and -susceptible T. ni larvae in midgut proteases, including caseinolytic proteolytic activity and zymogram profile and serine protease activities, in midgut aminopeptidase and alkaline phosphatase activity, and in midgut esterases and hemolymph plasma melanization activity. For analysis of genetic linkage of Cry2Ab resistance with potential Cry toxin receptor genes, molecular markers for the midgut cadherin, alkaline phosphatase (ALP), and aminopeptidase N (APN) genes were identified between the original greenhouse-derived dual-toxin-resistant and the susceptible laboratory T. ni strains. Genetic linkage analysis showed that the Cry2Ab resistance in T. ni was not genetically associated with the midgut genes coding for the cadherin, ALP, and 6 APNs (APN1 to APN6) nor associated with the ABC transporter gene ABCC2. Therefore, the Cry2Ab resistance in T. ni is conferred by a novel but unknown genetic mechanism.T he Gram-positive soil bacterium Bacillus thuringiensis (Bt) has been widely used as a microbial insecticide in sprayable formulations, and Bt toxins are the primary insecticidal proteins expressed in genetically engineered crops to confer insect resistance (1; ISAAA's GM Approval Database, http://www.isaaa.org /gmapprovaldatabase/). Since the mid-1990s, insect-resistant Bt crops have been rapidly adopted with proven economic and environmental benefits (2, 3). However, development of insect resistance to Bt toxins threatens the long-term success of application of Bt toxins for insect pest control. The genetic potential of insect populations to evolve Bt resistance has been well shown in laboratory selections, and cases of insect resistance to Bt formulations and Bt crops have occurred in insect populations under selection pressure by Bt sprays and Bt crops in the field (4-8).Studies of insect resistance to Bt toxins have so far been mostly on Lepidoptera pests to the toxin Cry1Ab or Cry1Ac (9-19), the two major Bt Cry toxins which are highly toxic to Lepidoptera pests and known to share the same binding sites in target insects (4, 20). Cry1Ab and Cry1Ac are the primary insecticidal proteins expressed in the current commercial transgenic Bt maize and Bt cotton varieties to target Lepidoptera pests in the field (21). Resistance to Cry1Ac and Cry1Ab ...

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“…The concerns regarding the environmental impact of GE plants include those worries related to their possible invasiveness in ecosystems (Snow et al 2005); outcrossing and horizontal gene transfer (Yao et al 2008, Rong et al 2010); development of resistant pest populations that would again require the input of pesticides (Tabashnik et al 2009); and effects on nontarget organisms (NTOs). In the case of IRGE plants, effects on NTOs is a particular concern, as these organisms provide important ecosystem services such as biological control (predators and parasitoids), pollination, and decomposition (Kennedy 2008, Romeis et al 2008a.…”

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confidence: 99%

Development of a Tier-1 Assay for Assessing the Toxicity of Insecticidal Substances Against <I>Coleomegilla maculata</I>

Ostrem

Romeis

et al. 2011

env. entom.

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To assess the potential dietary effects of insecticidal substances on the predacious ladybird beetle, Coleomegilla maculata De Geer, a Tier-1 laboratory testing system was developed. Artificial diets using shrimp eggs were developed, and a tier-1 bioassay examining C. maculata development and survival was designed based on those diets. To further measure the artificial diet in a Tier-1 testing system, larvae of C. maculata were fed the diet treated with different concentrations of an inorganic stomach poison, potassium arsenate (PA), or a cysteine protease inhibitor, E-64. The results demonstrated that the testing system was capable of detecting the dietary effects of both substances on the survival and development ofC. maculata. With increasing concentrations of PA in the diet, fewer larvae developed to adults, with only 22.7% larvae surviving to the adult stage in the treatment with the highest content of PA (32 µg/g of diet). Likewise, dose-dependent responses also were found for other life-table parameters of C. maculata. Similar to the assays with PA, the survival rates of C. maculata consistently decreased with increasing E-64 content in the diet. Survival analysis showed that the insects fed E-64 at 50, 150, and 450 µg/g in the diet had significantly lower survival rates compared with those on the untreated artificial diet. The study presented here describes a robust testing system that will be useful for assessing the potential hazard (or toxicity) effects after dietary exposure of insecticidal compounds produced by GE plants or conventional insecticides on the ladybird predator, C. maculata. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ABSTRACT To assess the potential dietary effects of insecticidal substances on the predacious ladybird beetle, Coleomegilla maculata De Geer, a Tier-1 laboratory testing system was developed. ArtiÞcial diets using shrimp eggs were developed, and a tier-1 bioassay examining C. maculata development and survival was designed based on those diets. To further measure the artiÞcial diet in a Tier-1 testing system, larvae of C. maculata were fed the diet treated with different concentrations of an inorganic stomach poison, potassium arsenate (PA), or a cysteine protease inhibitor, E-64. The results demonstrated that the testing system was capable of detecting the dietary effects of both substances on the survival and development of C. maculata. With increasing concentrations of PA in the diet, fewer larvae developed to adults, with only 22.7% larvae surviving to the adult stage in the treatment with the highest content of PA (32 g/g of diet). Likewise, dose-dependent responses also were found for other life-table parameters of C. maculata. Similar to the assays with PA, the survival rates of C. maculata consistently decreased with increasing E-64 content in the die...

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Asymmetrical cross-resistance betweenBacillus thuringiensistoxins Cry1Ac and Cry2Ab in pink bollworm

Cited by 115 publications

References 58 publications

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Interaction Patterns betweenPotato Virus Yand eIF4E-Mediated Recessive Resistance in the Solanaceae

Resistance to Bacillus thuringiensis Toxin Cry2Ab in Trichoplusia ni Is Conferred by a Novel Genetic Mechanism

Development of a Tier-1 Assay for Assessing the Toxicity of Insecticidal Substances Against <I>Coleomegilla maculata</I>

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