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«Proposal To Sequence the Genome of the Pea Aphid (Acyrthosiphon pisum) The International Aphid Genomics Consortium (IAGC) Steering Committee (in ...»

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Proposal To Sequence the Genome of the Pea Aphid (Acyrthosiphon pisum)

The International Aphid Genomics Consortium (IAGC) Steering Committee (in

alphabetical order): Marina Caillauda, Owain Edwardsb, Linda Fieldc, Danièle GiblotDucrayd, Stewart Graye, David Hawthornef, Wayne Hunterg, Georg Janderh, Nancy

Morani, Andres Moyaj, Atsushi Nakabachik, Hugh Robertsonl, Kevin Shufranm, JeanChristophe Simond, David Sternn, Denis Tagud

Contact: D. Stern; Ph. 609-258-0759; FAX 609-258-7892; dstern@princeton.edu Abstract We propose sequencing of the 300Mb nuclear genome of the pea aphid, Acyrthosiphon pisum. Aphids display a diversity of biological problems that are not easily studied in other genetic model systems. First, because they are the premier model for the study of bacterial endosymbiosis and because they vector many well-studied plant viruses, aphids are an excellent model for studying animal interactions with microbes.

Second, because their normal life cycle displays extreme developmental plasticity as well as both clonal and sexual reproduction, aphids provide the opportunity to understand the basis of phenotypic plasticity as well as the genomic consequences of sexual versus asexual reproduction. Their alternative reproductive modes can also be exploited in genetic experiments, because clones can be maintained indefinitely in the laboratory with sexual generations induced at will1,2. Third, aphids provide some of the best studied instances of adaptation, in the form of both insecticide resistance, which has evolved through several molecular mechanisms, and host plant adaptation, which has repeatedly generated novel aphid lineages specialized to particular crop plant cultivars and which is presumably the basis for the radiation of aphids onto many specialized host plants during their long evolutionary history. Finally, an aphid genome will provide important phylogenetic information, serving as an outgroup to the many genomes being sequenced in holometabolous insects (flies, beetles, bees, moths) and providing a valuable resource for annotation of the genomes of other hemimetabolous insects, most of which have much larger genomes than the aphid.

Aphid biology is relevant to human health in several ways. First, aphids cause crop damage on the order of hundreds of millions of dollars in lost production each year3,4. Second, pest aphid populations are controlled primarily by pesticides. These pesticides may persist on harvested crops and in the environment, to the detriment of human health and environmental quality. Third, bacterial symbiosis in aphids may serve as a general model for understanding processes of bacterial infection5-7. Fourth, aphids transmit some viruses in ways that resemble insect-borne human viruses and thus provide models for studying insect-vector viral disease8,9. Finally, because aphids display dramatic phenotypic plasticity10,11, they provide a model system for how environmental and genetic factors interact in determining the phenotype. There is growing awareness that phenotypic plasticity, for example differential response to drugs, is an important component of human welfare12.

As a group, aphids are among the most intensively studied insects and are the focus of a large community of researchers. Several labs have developed genomic tools for studying aphids, including genetic maps, BAC libraries, EST sequences and microarrays.

An aphid genome sequence would provide immediate benefits, including the bioinformatic discovery of many new potential targets for biological control. In addition, the pea aphid, with its relatively small genome compared to most hemimetabolous insects, will provide a valuable bioinformatics resource for annotating the genome of other hemimetabolous insects, including important vectors of human disease.

Summary of major benefits of a pea aphid genome

1. Model for interactions with micro-organisms a. Best-studied model of bacterial-animal endosymbiosis b. Excellent model of insect-vectored virus transmission

2. Model for developmental plasticity a. Displays many cases of extreme developmental plasticity b. Excellent model of origins of asexuality in an animal

3. Model of adaptation a. Insecticide resistance (leads to heavier insecticide use on crops) b. Host-plant adaptation – Excellent model of insect-plant interactions, with genomic resources available for plant

4. Comparative genomics a. Hemimetabolous genome provides an outgroup to all other holometabolous insects b. Small aphid genome provides an important resource for annotation of other hemimetabolous insects that often have much larger genomes.

Other hemimetabolous insects include many other agricultural pests and human disease vectors.

Rationale for choice of Pea Aphid for genome sequencing Approximately 4,000 species of aphids have been described, but only a few species have been adopted for laboratory study. The IAGC believes that the genome should be sequenced for one species, the pea aphid (Acyrthosiphon pisum), which is the primary species used in laboratory and genetic studies.

Closely related species are major agricultural pests A. pisum is a member of the Aphidinae, which includes almost all aphid pest species, and specifically of the largest aphid tribe, the Macrosiphini, which includes both most important aphid agricultural pests, including the peach-potato aphid (Myzus persicae) and the Russian wheat aphid (Diuraphis noxia), and most species used in laboratory studies. Nucleotide divergences for sequenced open reading frames of orthologous genes range from 5% to 10% in comparisons of A. pisum to other Macrosiphini and up to 15% for comparisons to other Aphidinae13,14. These values indicate less divergence than for human-mouse (78% identity of orthologs) and far less than for mosquito-Drosophila (56% identity of orthologs). Assuming that rates of nucleotide divergence and genomic rearrangements are similarly correlated in aphids and other animals, these values are a strong indicator that A. pisum will show substantial synteny of gene order and orientation with other Aphidinae. For example, over 90% of human and mouse genes are estimated to fall within chromosome blocks that are syntenic for these two species, and even mosquito-Drosophila genomes show considerable regions of synteny. Given the much lower levels of sequence divergence among Aphidinae, the prospects are excellent for being able to extend genomic information from A. pisum to other aphid species. Furthermore, no genome sequencing efforts have been initiated for any member of the larger insect clade containing aphids, the Hemiptera, which contains many additional major agricultural pests (whiteflies, scale insects, planthoppers, and leafhoppers) and vectors of human disease (Rhodnius). The A. pisum sequence would undoubtedly be useful to researchers working on those insects.

Major benefits of choosing the pea aphid, Acyrthosiphon pisum A. pisum is the primary aphid used in laboratory studies due to its relatively large size and the simplicity of rearing. Unlike many aphid species, A. pisum can be reared through the entire life cycle on a single host plant, and methods for rearing this aphid in Petri dishes on excised leaves or on artificial diets have been developed15-17. Genetic maps are available2, and efforts are underway to perform transgenesis and RNA interference. There are extensive data on the genomics and physiology of the endosymbionts18,19. Many races of A. pisum can be found in the wild that differ in their host plant preferences, and some of these races represent incipient speciation events1,2. A.

pisum can be raised in the lab on many host plants, including the genomic model system Medicago truncatula.

Genome size and other relevant genetic data A. pisum has a haploid genome size of approximately 300Mb20 (www.genomesize.com) on four holocentric chromosomes. This genome size estimate has been confirmed by J. Spencer Johnston at Texas A&M. Chromosome in situ hybridization has been developed21, which will allow assignment of BAC clones, and therefore physical maps and the complete genome, to chromosomes.

Major research areas that will be influenced by a pea aphid genome sequence Aphids are used to investigate many biological questions in fields as diverse as genetics, physiology, agriculture, microbiology, virology, ecology, evolution, development and behavior. Here we review the major fields of enquiry that we expect will be influenced by the sequencing of the pea aphid genome and indicate some of the immediate uses of an aphid genome.

1 – Interactions with micro-organisms

1.a – Bacterial Symbiosis Aphids provide the best-studied model for maternally transmitted symbionts, and aphid-bacterial symbioses are a prime illustration of the progress possible using genomic approaches. Aphids display highly coevolved, ancient, mutualistic intracellular symbiosis as well as more recent, conditionally beneficial and facultative associations and pathogenesis.

Obligate primary symbiosis in aphids: The primary symbiont of aphids, Buchnera aphidicola, is maternally transmitted, inhabits specialized cells (bacteriocytes), and is required for host development, growth and reproduction. The Buchnera genome has undergone massive reduction, as is typical of endosymbiotic lineages. Three Buchnera genomes have been sequenced18,22,23 and they contain only 0.61-0.65 Mb, encoding just 510-570 proteins; another Buchnera, now being sequenced by Moya et al in Spain, is the smallest known bacterial genome at 0.45 Mb. The close relationship of Buchnera to E.

coli and to other fully sequenced and well-studied bacteria has enabled the inference of function for about 90% of Buchnera genes. The gene inventories have confirmed and extended experimental data showing that Buchnera is able to provision its hosts with nine essential amino acids that are limiting in the phloem sap diet24.

Buchnera also affects aspects of aphid biology other than nutrition. For example, the sensitivity of aphids to heat, a major factor determining their geographic and seasonal distributions, can be ascribed in large part to heat sensitivity of Buchnera23,25. Heat shock genes are expressed at very high levels in Buchnera even in the absence of thermal stress, possibly to mask effects of mutations that affect protein stability. One of these, the chaperonin GroEL, is present in the aphid hemocoel, where it has been shown to provide protection to plant-pathogenic viruses that are vectored by the aphids26.

Although the genomic studies of Buchnera provide some answers to how this intimate symbiosis functions, they also raise several questions for which answers cannot be obtained without information from the host genome. Buchnera lacks many genes that would appear to be essential to bacterial function, including most genes responsible for phospholipid biosynthesis, implying that Buchnera cannot synthesize its own cell membrane. Most genes encoding transcriptional regulators are also missing from the Buchnera genomes, making it unclear how Buchnera regulates its activities with the host.

Facultative symbiosis in aphids: Aphids can also contain any of several maternally inherited symbiotic lineages that coexist with Buchnera27-31. For example, naturally occurring strains of A. pisum can contain any of three gamma-proteobacterial symbiont lineages (or none), as well as Rickettsia and Spiroplasma species; these organisms are also found in other aphid species and other insect groups, where they are known to disrupt sex ratios.

The more recent, facultative symbionts of aphids provide examples of the transition between pathogenic and harmless or mutualistic interactions7. For example, the gamma-proteobacterial symbionts have been shown experimentally to confer hosts with increased tolerance to heat stress and with the ability to overcome and kill internally developing parasitoid wasps32,33. They are closely related to human pathogens such as Yersinia pestis (the agent causing plague), Escherichia coli, and Salmonella (causing typhus), and they contain some of the same genes implicated in pathogenesis, such as a homolog of the Shiga toxin (van der Wilk et al 1999). Therefore, these symbionts serve as excellent models for studying bacterial infection and the early evolutionary stages of symbiosis.

1.b - Virus infection A number of viruses, including both RNA and DNA viruses, have been characterized in aphids, and specifically in A. pisum. Several of these genomes have been sequenced and biological effects have been evaluated. These viruses vary in host range, mode of transmission, and effects on hosts, which range from innocuous to extreme pathogenesis34-37. These provide potential viral models for studies of the mechanisms and dynamics of infectious disease.

1.c – Plant virus vectoring Viruses are obligate parasites that are unable to survive outside their hosts. In contrast to animal and insect viruses, plant viruses must be vectored from one immobile host to another and aphids vector hundreds of plant viruses9,38.

Virus transmission is directly related to aphid feeding. Aphids have piercingsucking mouthparts and their feeding behavior consists of probing plant epidermal tissues and ingesting phloem sap. Virus particles can be transmitted in either a circulative or non-circulative manner. In both cases, virus transmission relies on specific interactions between virus and aphid molecules.

The majority of plant viruses are transmitted in a non-circulative (non-persistent) manner. Acquisition from an infected plant requires an association of virus particles with aphid mouthparts and the anterior part of the alimentary tract39. Virus particles are released in subsequent probing by the aphid and can thus be transferred to uninfected plants. Non-circulative transmission relies on both virus and aphid genetic properties40, and specific epitopes on viral coat proteins are required for attachment to aphid mouthparts41,42.

During circulative (persistent) transmission, virus particles cross aphid cell membranes, apparently through a receptor-assisted endocytosis-exocytosis mechanism40,43,44. Virus particles pass through the aphid gut and hemocoel to the accessory salivary gland to facilitate transmission to a plant via the saliva9. Aphid proteins that are linked to transmission efficiency have been found; some of these proteins are able to specifically bind transmissible virus particles and may therefore represent putative virus receptors45. Furthermore, genetic crosses have demonstrated that the genotype of the aphid facilitates the transmission of virus46.

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