Genome sequence of the pea aphid Acyrthosiphon pisum

Richards S, Gibbs RA, Gerardo NM, Moran N, Nakabachi A, Stern D, Tagu D, Wilson AC, Muzny D, Kovar C, Cree A, Chacko J, Chandrabose MN, Dinh HH, Gabisi RA, Hines S, Hume J, Jhangian SN, Joshi V, Lewis LR, Liu YS, Lopez J, Morgan MB, Nguyen NB, Okwuonu GO, Ruiz SJ, Santibanez J, Wright RA, Fowler GR, Hitchens ME, Lozado RJ, Moen C, Steffen D, Warren JT, Zhang J, Nazareth LV, Chavez D, Davis C, Lee SL, Patel BM, Pu LL, Bell SN, Johnson AJ, Vattathil S, Williams RL Jr, Shigenobu S, Dang PM, Morioka M, Fukatsu T, Kudo T, Miyagishima SY, Jiang H, Worley KC, Legeai F, Gauthier JP, Collin O, Zhang L, Chen HC, Ermolaeva O, Hlavina W, Kapustin Y, Kiryutin B, Kitts P, Maglott D, Murphy T, Pruitt K, Sapojnikov V, Souvorov A, Thibaud-Nissen FF, Câmara F, Guigó R, Stanke M, Solovyev V, Kosarev P, Gilbert D, Gabaldón T, Huerta-Cepas J, Marcet-Houben M, Pignatelli M, Moya A, Rispe C, Ollivier M, Quesneville H, Permal E, Llorens C, Futami R, Hedges D, Robertson HM, Alioto T, Mariotti M, Nikoh N, McCutcheon JP, Burke G, Kamins A, Latorre A, Moran NA, Ashton P, Calevro F, Charles H, Colella S, Douglas A, Jander G, Jones DH, Febvay G, Kamphuis LG, Kushlan PF, Macdonald S, Ramsey J, Schwartz J, Seah S, Thomas G, Vellozo A, Cass B, Degnan P, Hurwitz B, Leonardo T, Koga R, Altincicek B, Anselme C, Atamian H, Barribeau SM, de Vos M, Duncan EJ, Evans J, Gabaldon T, Ghanim M, Heddi A, Kaloshian I, Vincent-Monegat C, Parker BJ, Pérez-Brocal V, Rahbé Y, Spragg CJ, Tamames J, Tamarit D, Tamborindeguy C, Vilcinskas A, Bickel RD, Brisson JA, Butts T, Chang CC, Christiaens O, Davis GK, Duncan E, Ferrier D, Iga M, Janssen R, Lu HL, McGregor A, Miura T, Smagghe G, Smith J, van der Zee M, Velarde R, Wilson M, Dearden P, Edwards OR, Gordon K, Hilgarth RS, Rider SD Jr, Srinivasan D, Walsh TK, Ishikawa A, Jaubert-Possamai S, Fenton B, Huang W, Rizk G, Lavenier D, Nicolas J, Smadja C, Zhou JJ, Vieira FG, He XL, Liu R, Rozas J, Field LM, Ashton PD, Campbell P, Carolan JC, Douglas AE, Fitzroy CI, Reardon KT, Reeck G, Singh K, Wilkinson TL, Huybrechts J, Abdel-latief M, Robichon A, Veenstra JA, Hauser F, Cazzamali G, Schneider M, Williamson M, Stafflinger E, Hansen KK, Grimmelikhuijzen CJ, Price DR, Caillaud M, van Fleet E, Ren Q, Gatehouse JA, Brault V, Monsion B, Diaz J, Hunnicutt L, Ju HJ, Pechuan X, Aguilar J, Cortés T, Ortiz-Rivas B, Martínez-Torres D, Dombrovsky A, Channels I, Dale RP, Davies TG, Williamson MS, Jones A, Sattelle D, Williamson S, Wolstenholme A, Reeck GR, Cottret L, Sagot MF, Heckel DG, Hunter W

PLoS Biology (Impact Factor: 12.69). 01/2009; e1000313.

ABSTRACT 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.

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    ABSTRACT: The primary endosymbionts of aphids are maternally inherited bacteria that live only within specialized host cells. Phylogenetic analysis of the 16S ribosomal DNA sequences of aphid endosymbionts reveals that they are a monophyletic group with a phylogeny completely concordant with that of their hosts, implying long-term cospeciation. Here we show that rates of base substitution are similar in the 16S ribosomal DNA of different endosymbiont lineages. In addition, we calibrate these rates by assigning age estimates for ancestral aphid hosts to the corresponding endosymbionts. The resulting rate estimates (1-2% per 50 Ma) are among the most reliable available for prokaryotes. They are very near values previously conjectured by using more tenuous assumptions for dating divergence events in eubacteria. Rates calibrated using dates inferred from fossil aphids imply that Asian and American species of the aphid tribe Melaphidina diverged by the early Eocene; this result confirms an earlier hypothesis based on biogeographic evidence. Based on these rate estimates, the minimum age of this endosymbiotic association and the age of aphids as a whole is estimated at 160-280 Ma.
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    ABSTRACT: Animals generally require a dietary supply of various nutrients (vitamins, essential amino acids, etc.) because their biosynthetic capabilities are limited. The capacity of aphids to use plant phloem sap, with low essential amino acid content, has been attributed to their symbiotic bacteria, Buchnera aphidicola, which can synthesize these nutrients; but this has not been demonstrated empirically. We demonstrate here that phloem sap obtained from the severed stylets of pea aphids Acyrthosiphon pisum feeding on Vicia faba plants generally provided inadequate amounts of at least one essential amino acid to support aphid growth. Complementary analyses using aphids reared on chemically defined diets with each amino acid individually omitted revealed that the capacity of the symbiotic bacterium B. aphidicola to synthesize essential amino acids exceeded the dietary deficit of all phloem amino acids except methionine. It is proposed that this shortfall of methionine was met by aphid usage of the non-protein amino acid 5-methylmethionine in the phloem sap. This study provides the first quantitative demonstration that bacterial symbiosis can meet the nutritional demand of plant-reared aphids. It shows how symbiosis with micro-organisms has enabled this group of animals to escape from the constraint of requiring a balanced dietary supply of amino acids.
    Proceedings of the Royal Society B: Biological Sciences 01/2009; 276(1658):987-91. · 5.68 Impact Factor
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    ABSTRACT: Aphids engage in symbiotic associations with a diverse assemblage of heritable bacteria. In addition to their obligate nutrient-provisioning symbiont, Buchnera aphidicola, aphids may also carry one or more facultative symbionts. Unlike obligate symbionts, facultative symbionts are not generally required for survival or reproduction and can invade novel hosts, based on both phylogenetic analyses and transfection experiments. Facultative symbionts are mutualistic in the context of various ecological interactions. Experiments on pea aphids (Acyrthosiphon pisum) have demonstrated that facultative symbionts protect against entomopathogenic fungi and parasitoid wasps, ameliorate the detrimental effects of heat, and influence host plant suitability. The protective symbiont, Hamiltonella defensa, has a dynamic genome, exhibiting evidence of recombination, phage-mediated gene uptake, and horizontal gene transfer and containing virulence and toxin-encoding genes. Although transmitted maternally with high fidelity, facultative symbionts occasionally move horizontally within and between species, resulting in the instantaneous acquisition of ecologically important traits, such as parasitoid defense.
    Annual Review of Entomology 10/2009; 55:247-66. · 13.59 Impact Factor


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Jun 19, 2013