Journal Article

Gene amplification and microsatellite polymorphism underlie a recent insect host shift

Zimmer, Christoph T., Nauen, Ralf, Wondji, Charles S., Field, Linda M., Bass, Chris, Kaussmann, Martin, Williamson, Martin S., Riveron, Jacob M., Wilding, Craig S.

2013

Overview

Host plant shifts of herbivorous insects may be a first step toward sympatric speciation and can create new pests of agriculturally important crops; however, the molecular mechanisms that mediate this process are poorly understood. Certain races of the polyphagous aphid Myzus persicae have recently adapted to feed on tobacco (Myzus persicae nicotianae) and show a reduced sensitivity to the plant alkaloid nicotine and cross-resistance to neonicotinoids a class of synthetic insecticides widely used for control. Here we show constitutive overexpression of a cytochrome P450 (CYP6CY3) allows tobacco-adapted races of M. persicae to efficiently detoxify nicotine and has preadapted them to resist neonicotinoid insecticides. CYP6CY3, is highly overexpressed in M. persicae nicotianae clones from three continents compared with M. persicae s.s. and expression level is significantly correlated with tolerance to nicotine. CYP6CY3 is highly efficient (compared with the primary human nicotine-metabolizing P450) at metabolizing nicotine and neonicotinoids to less toxic metabolites in vitro and generation of transgenic Drosophila expressing CYP6CY3 demonstrate that it confers resistance to both compounds in vivo. Overexpression of CYP6CY3 results from the expansion of a dinucleotide microsatellite in the promoter region and a recent gene amplification, with some aphid clones carrying up to 100 copies. We conclude that the mutations leading to overexpression of CYP6CY3 were a prerequisite for the host shift of M. persicae to tobacco and that gene amplification and microsatellite polymorphism are evolutionary drivers in insect host adaptation.

• Publisher: National Academy of Sciences,NATIONAL ACADEMY OF SCIENCES,National Acad Sciences
• Subject: Adaptation, Biological - genetics / Animals / Aphididae / Aphids - drug effects / Aphids - enzymology / Aryl Hydrocarbon Hydroxylases - metabolism / Base Sequence / Biological Sciences / Chromatography, Liquid / clones / crops / cross resistance / cytochrome P-450 / Cytochromes / Dinucleotide Repeats - genetics / Drosophila / gene amplification / Gene Amplification - genetics / Gene expression / gene overexpression / genetically modified organisms / Herbivores / host plants / Host-Parasite Interactions / humans / Insect genetics / Insect pests / Insecticides / Insects / Metabolism / Metabolites / microsatellite repeats / Microsatellites / Molecular Sequence Data / Mortality / mutation / Mutation - genetics / Myzus persicae / Myzus persicae nicotianae / neonicotinoid insecticides / Nicotiana - parasitology / Nicotine / Nicotine - toxicity / pests / phytophagous insects / Polymerase chain reaction / Polymorphism / Polymorphism, Genetic - genetics / Promoter regions / races / Real-Time Polymerase Chain Reaction / Sequence Analysis, DNA / Speciation / sympatric speciation / Tandem Mass Spectrometry / Tobacco / Tobacco industry / toxicity / Transgenic insects