Award details

Functional genomics of aphid adaption to plant defenses

Reference	BB/L001985/1
Principal Investigator / Supervisor	Dr David Swarbreck
Co-Investigators / Co-Supervisors
Institution	Earlham Institute
Department	Research Faculty
Funding type	Research
Value (£)	276,863
Status	Completed
Type	Research Grant
Start date	03/03/2014
End date	02/09/2017
Duration	42 months

Abstract

The green peach aphid (GPA) Myzus persicae is an agronomically important pest worldwide. This aphid colonizes over 400 different plant species from more than 50 plant families and has developed resistance to all insecticides that are currently in use. Remarkably, a single GPA clone (consisting of genetically identical individuals) can colonize diverse plant species of several plant families, whilst the specialist pea aphid Acyrthosiphon pisum (for which the genome sequence is available) consists of genetically distinct races each of which colonizes different plant species of the family Fabaceae (or Leguminosae). The objective of this project is to identify mechanisms that have given GPA its impressive phenotypic plasticity. We will test the hypothesis that some gene families have adaptively expanded, offering GPA better protection to phytochemicals and insecticides. Given that genetically identical clones can exploit distinct host plants, we hypothesize that epigenetic regulation affects gene expression levels, and that certain gene members within these gene families are differentially up or down-regulated depending on exposure to host species and insecticides. This project tests an exiting new idea that adaptive gene duplication and expansion of certain gene families has provided GPA with a versatile "genetic toolbox" allowing for a phenotypically plastic response through epigenetic regulation, thereby equipping this parasite with a vast evolutionary potential that could threaten future food security. We will use state-of-the-art genomics tools to compare aphid genomes and assess gene expression and DNA methylation profiles of GPA reared on diverse plant species and exposed to insecticides with different chemistries. We will then knock down the expression of specific GPA genes to study their effect on GPA adaptation to plants and insecticides. This project includes a translational component that will be taken forward in collaboration with Syngenta.

Summary

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 membersof 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.

Impact Summary

The green peach aphid (GPA) Myzus persicae is one of the most notorious plant pests worldwide for various reasons. First, this insect transmits more than 100 different plant viruses, which can cause dramatic yield losses in crops. One example is Turnip yellows virus (TuYV), which is thought to reduce yield of oilseed rape by up to 30% in the UK. Secondly, GPA can colonize over 400 different plant species, including important crops such as oilseed rape, beet, tomato and potato, and wild plant species, which may serve as sources of the plant viruses. As well, GPA has developed resistance to over 70 different synthetic compounds. This, coupled with changes in the regulatory landscape on pesticide usage, has resulted in the neonicotinoids class of pesticides being one of few left that successfully controls these insects. In addition, climate change has contributed to the insect pest emerging several weeks earlier in annual crop growing seasons, exacerbating crop losses and affecting in particular the temperate regions in Europe, including the UK. Finally, intensification and globalization of agriculture has contributed to new introductions of insect pests (including insecticide-resistant GPA clones) and vectored viruses into production fields worldwide. The research described in this proposal will use state-of-the-art technologies and novel approaches to increase the likelihood of making fundamental discoveries that will underpin the development of new strategies to control this notorious pest in the future. Therefore, this project addresses two of the BBSRC key priorities - 'Living with Environmental Change' and 'Crop Science'. This project could inform industry and strategic research programs that focus on the identification of new pest control methods on four accounts. First, genome sequence information of various clones and RNAi technology will identify GPA genes involved in insecticide resistance. This information can be used for the generation of markers for thedetection of insecticide-resistant GPA in the field. Furthermore, the described research enables assessment of the role of GPA genes in GPA-plant interactions, which could inform plant-breeding strategies for increasing plant resistance to GPA and other aphids. As well, this project may identify targets in GPA for aphid control e.g. new targets for biochemical control or control via in planta RNAi. Finally, it will elucidate the role of epigenetic regulation in GPA development and phenotypic plasticity leading possibly to novel control targets of GPA. Syngenta has acknowledged the strategic importance of this research by supporting this proposal as an Industrial Partnership Award (IPA). A good working relationship between PI Hogenhout and Syngenta colleagues at Jealott's Hill has already led to the sharing of information and the establishment of new protocols at Syngenta. Intellectual property (IP) will be managed by the Plant Bioscience Limited (PBL), which is an independent technology management company specializing in plant, food and microbial science based that manages IP at the Norwich Research Park. The proposed research will aid other strategic research projects of the Hogenhout lab, such as understanding the mechanisms involved in GPA transmission of viruses, including TuYV (funded by a CASE studentship), and whole-genomics approaches to understand the interactions of whiteflies, which are sister species of aphids, with plants (funded by the Gates foundation). We will communicate science to the general public. The three team leaders will host Nuffield scholars and we will, in coordination with Dr. Ian Bedford (Manager of the Insectary at JIC), organize plant pest and disease clinics. As well, we will participate in 'Science Camps' for high school students, converse achievements relevant for press releases and general public engagement (JIC Press Office) and join in knowledge exchange and commercialization (KEC) activities at the JIC.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Crop Science, Plant Science
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	Industrial Partnership Award (IPA)

Associated awards:

BB/L002108/1 Functional Genomics of Aphid Adaptation to Plant Species

BB/L002302/1 Functional genomics of aphid adaption to plant defenses

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