Functional Genomics of Aphid Adaptation to Plant Species

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1. The Background: The green peach aphid (GPA) Myzus persicae, an agronomically important pest worldwide, can colonize over 400 different plant species from more than 50 plant families and holds the world record of insecticide resistance mechanisms, showing resistance to at least 70 different synthetic compounds. Moreover, GPA is remarkably plastic such that one clone consisting of genetically identical females can survive and reproduce on a wide range of plant species. This is in contrast to majority of other aphid species, including the pea aphid (Acyrthosiphon pisum), which has adapted to one or a few related plant species within one plant family.2. The Big Questions: What are the genetic control mechanisms that underlie the phenotypic plasticity of GPA? Is this plasticity related to GPA ability to evolve insecticide resistance to at least 70 different synthetic compounds in the last 60 years, i.e. an "evolutionary blink-of-an-eye"?3. The Hypotheses: We hypothesize that the phenotypic plasticity of GPA is due to its (1) genomic adaptations in the form of the expansion of certain multigene families that are important for virulence, in combination with (2) epigenetic regulation affecting gene expression levels of gene family members. Depending on exposure to plant hosts and pesticides, certain members within gene families are differentially up or down-regulated, providing the parasite with a versatile "genetic toolbox".4. The Supportive Data: The Hogenhout lab has developed research tools for GPA clone "O", which has predominated in the UK, causing damage to diverse crops in recent years. We maintain this clone as genetically identical females that can survive and reproduce on diverse plant species, including for example Chinese cabbage and tobacco plants, which produce different defense compounds that are toxic to aphids. The GPA clone O whole genome sequence is currently being assembled and annotated using gene expression data. We have evidence that members of specific gene families, such as cathepsins and cuticular proteins, play a role in the phenotypic adaptation of GPA to plant species. We are also interested in cytochrome 450 monooxygenases (P450s), which are detoxification enzymes of organic substances such as phytochemicals and pesticides. Finally, we have developed the plant-mediated RNA interference (RNAi) technology enabling studies of the effect of the knock down of specific GPA genes on GPA survival and reproduction on various plant species.5. The Objectives:In the first objective we will advance the construction of a physical genomic map, identify coding sequences and conduct evolutionary analysis of gene family members of GPA clone O. In the second objective we will assess which genes are differentially regulated in GPA clone O reared on different plant species and exposed to various pesticides. We will also sequence the genomes of additional GPA clones that are susceptible and resistant to pesticides and determine if differentially expressed genes are subject to high mutation frequencies. In the third objective we use plant-mediated RNAi to knock down the expression of specific genes to assess their effect on the ability of GPA to survive on different plant species and upon insecticide exposure. We will assess if DNA methylation is involved in GPA phenotypic plasticity. 6. The Implications: At completion of this project we will have gained a better understanding of how GPA adapts to multiple plant species and if this relates to mechanisms involved in the development of insecticide resistance of GPA. We will also have elucidated the level of genomic variation amongst GPA clones susceptible and resistant to pesticides. This research is fundamentally important to our overall understanding of how insect adapt to their environments. Ultimately, this could have practical implications for the increasing problem of the evolution of insecticide resistance in crop-pest control.