Aphid's Genome Reflects Its Reproductive, Symbiotic Lifestyle
ScienceDaily (Feb. 23, 2010) — Aphids could be considered the "mosquitoes" of the plant world, depending on the "blood" of plants to survive. They live in symbiosis with bacteria that pass from one generation to the next, producing essential amino acids. Aphids with the same genotype can be wingless or winged. In different seasons, they develop as asexual females who produce offspring with identical genes through parthenogenesis. When temperatures drop, they can give birth to males who then fertilize the eggs laid by females.
Colony of young aphids. (Credit: iStockphoto/Michael Pettigrew)
"Because this is a different kind of insect -- not a fruit fly, not a beetle, not a hymenoptera (butterfly and moth) -- we are seeing things that people have not seen in other projects," Richards said.
Dr. David Stern, professor of ecology and evolutionary biology at Princeton University, said that even though he pushed hard to get the aphid genome sequenced, "it turned out to be far more interesting than I was expecting."
He agreed with Richards that the aphid presents a special case.
"Look at this little insect, sitting on a plant and sucking plant juices. You don't realize that it is involved in a historic battle with plants for access to its life blood. All its genes have evolved to allow it to exploit its feeding relationship," said Stern.
"We found a lot of genes -- 35,000 compared to 15,000 to 20,000 in other insects and 25,000 in humans," said Richards, a corresponding author of the paper.
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Abstract Top
Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.
Author Summary
Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.
Author Summary
Aphids are common pests of crops and ornamental plants. Facilitated by their ancient association with intracellular symbiotic bacteria that synthesize essential amino acids, aphids feed on phloem (sap). Exploitation of a diversity of long-lived woody and short-lived herbaceous hosts by many aphid species is a result of specializations that allow aphids to discover and exploit suitable host plants. Such specializations include production by a single genotype of multiple alternative phenotypes including asexual, sexual, winged, and unwinged forms. We have generated a draft genome sequence of the pea aphid, an aphid that is a model for the study of symbiosis, development, and host plant specialization. Some of the many highlights of our genome analysis include an expanded total gene set with remarkable levels of gene duplication, as well as aphid-lineage-specific gene losses. We find that the pea aphid genome contains all genes required for epigenetic regulation by methylation, that genes encoding the synthesis of a number of essential amino acids are distributed between the genomes of the pea aphid and its symbiont, Buchnera aphidicola, and that many genes encoding immune system components are absent. These genome data will form the basis for future aphid research and have already underpinned a variety of genome-wide approaches to understanding aphid biology.
Citation: The International Aphid Genomics Consortium (2010) Genome Sequence of the Pea AphidAcyrthosiphon pisum. PLoS Biol 8(2): e1000313. doi:10.1371/journal.pbio.1000313
Academic Editor: Jonathan A. Eisen, University of California Davis, United States of America
Received: May 29, 2009; Accepted: January 19, 2010; Published: February 23, 2010
This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Funding: Work at the Baylor Medical College Human Genome Sequencing Center was funded by grant 5-U54-HG003273 from the National Human Genome Research Institute. AphidBase is supported with funding from the French National Institute for Agricultural Research (INRA) and the French National Institute for Research in Computer Science and Control (INRIA). Pea Aphid Genome Annotation Workshop I was supported by an American Genetic Association Special Event Award and an NRI, US Department of Agriculture Cooperative State Research, Education, and Extension Service 2007-04628 award to ACCW. FgenesH models were donated by Softberry, Inc. This research was additionally supported in part by the Intramural Research Program of the NIH, National Library of Medicine. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: AMP, antimicrobial peptide; CBD, chitin-binding domain; CCEs, carboxyl/choline esterases; CSPs, chemosensory proteins; GPCR, G protein-coupled receptor; GRs, gustatory receptors; GSTs, glutathione S-transferases; JH, juvenile hormone; MFS, major facilitator superfamily; ML, Maximum Likelihood; NJ, Neighbor Joining; OBPs, odorant-binding proteins; Ors, odorant receptors; P450s, P450 monooxygenases; PGRPs, peptidoglycan recognition proteins; RBH, reciprocal best hit; RISC, RNA Induced Silencing Complex; TE, transposable element
* E-mail: stephenr@bcm.tmc.edu
¶ Membership of the International Aphid Genomics Consortium is provided in the Acknowledgments.
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