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1. Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria.

Author

Chandler SM, Wilkinson TL, and Douglas AE

Subjects
Analysis of Variance, Animals, DNA Primers genetics, Polymerase Chain Reaction, RNA, Ribosomal, 16S, Amino Acids analysis, Aphids microbiology, Enterobacteriaceae genetics, Lamiaceae, Phloem chemistry, Symbiosis, Vicia faba
Abstract

The interactions between herbivorous insects and their symbiotic micro-organisms can be influenced by the plant species on which the insects are reared, but the underlying mechanisms are not understood. Here, we identify plant nutrients, specifically amino acids, as a candidate factor affecting the impact of symbiotic bacteria on the performance of the phloem-feeding aphid Aphis fabae. Aphis fabae grew more slowly on the labiate plant Lamium purpureum than on an alternative host plant Vicia faba, and the negative effect of L. purpureum on aphid growth was consistently exacerbated by the bacterial secondary symbionts Regiella insecticola and Hamiltonella defensa, which attained high densities in L. purpureum-reared aphids. The amino acid content of the phloem sap of L. purpureum was very low; and A. fabae on chemically defined diets of low amino acid content also grew slowly and had elevated secondary symbiont densities. It is suggested that the phloem nutrient profile of L. purpureum promotes deleterious traits in the secondary symbionts and disturbs insect controls over bacterial abundance.

Published
2008
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2. Role of host nutrition in symbiont regulation: impact of dietary nitrogen on proliferation of obligate and facultative bacterial endosymbionts of the pea aphid Acyrthosiphon pisum.

Author

Wilkinson TL, Koga R, and Fukatsu T

Subjects
Animals, Aphids physiology, Pisum sativum parasitology, Aphids microbiology, Bacterial Physiological Phenomena, Nitrogen pharmacology, Serratia physiology, Symbiosis physiology
Abstract

The impact of host nutrition on symbiont regulation in the pea aphid Acyrthosiphon pisum was investigated. The population density of the obligate symbiont Buchnera aphidicola positively correlated with dietary nitrogen levels. In contrast, the population density of the facultative symbiont Serratia symbiotica increased in aphids reared on low-nitrogen diets, indicating distinct regulatory mechanisms in the same insect host.

Published
2007
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3. The impact of host plant on the abundance and function of symbiotic bacteria in an aphid.

Author

Wilkinson TL, Adams D, Minto LB, and Douglas AE

Subjects
Amino Acids analysis, Amino Acids biosynthesis, Amino Acids metabolism, Animals, Aphids growth & development, Aphids metabolism, Buchnera metabolism, Colony Count, Microbial, Fabaceae metabolism, Lamiaceae metabolism, Aphids microbiology, Buchnera physiology, Fabaceae parasitology, Lamiaceae parasitology, Papaver parasitology, Symbiosis
Abstract

The black-bean aphid Aphis fabae bears populations of coccoid symbiotic bacteria Buchnera spp. at 2.0-3.2 x 10(7)cells mg(-1)aphid mass and rod-shaped secondary symbionts of uncertain taxonomic affiliation at 0.1-0.6 x 10(7)cells mg(-1)aphid mass. Buchnera provides essential amino acids, supplementing the poor supply in the aphid diet of plant phloem sap. Comparison of the performance of A. fabae containing and experimentally deprived of their bacteria showed that the bacteria caused increased larval mass of aphids reared on Chenopodium album and Papaver dubium plants, but not when reared on Lamium purpureum. In the aphids reared on L. purpureum, the density of the bacteria, especially the secondary symbionts, was significantly elevated, and bacterial-mediated production of the essential amino acid threonine was reduced, even though the essential amino acid content of phloem exudates from L. purpureum had a low threonine content. It is proposed that the shortfall in threonine, possibly compounded by the high density of secondary symbionts, may contribute to the poor performance of the aphids on L. purpureum. This study offers the first evidence to suggest plant-mediated interference with the nutritional function of symbiotic bacteria in any phytophagous insect.

Published
2001
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4. Quantifying nutrient production by the microbial symbionts in an aphid.

Author

Douglas AE, Minto LB, and Wilkinson TL

Subjects
Amino Acids, Essential metabolism, Animal Nutritional Physiological Phenomena, Animals, Aphids growth & development, Diet, Insect Proteins biosynthesis, Larva growth & development, Larva metabolism, Larva microbiology, Plants, Aphids metabolism, Aphids microbiology, Buchnera metabolism, Symbiosis
Abstract

The symbiotic bacteria Buchnera sp. provide aphids with essential amino acids, nutrients in short supply in the aphid diet of plant phloem sap. The contribution of Buchnera-derived amino acids to net protein growth of the aphid Aphis fabae was quantified from the protein growth of aphids reared on chemically defined diets lacking individual amino acids. The amino acid production rates varied among the nine essential amino acids over the range 8-156 pmol microg(-1)protein day(-1) (for tryptophan and leucine, respectively), equivalent to 0.02-0.33 fmol Buchnera(-1)day(-1). In a complementary metabolic analysis, the aphids incorporated radioactivity from dietary [(14)C]glutamic acid into the essential amino acids isoleucine, lysine and threonine. Incorporation into isoleucine was significantly elevated by the omission of dietary isoleucine, indicating that dietary supply may affect the biosynthetic rates of certain amino acids by Buchnera. Aphids experimentally deprived of Buchnera did not synthesize essential amino acids from dietary glutamic acid. The mortality of aposymbionts was high over 7 days on the phenylalanine-free diet, and their assimilation of dietary leucine was depressed on the complete diet, suggesting that both the absence of bacteria-derived amino acids and the low rates of assimilation of certain dietary amino acids may contribute to the poor growth of these insects.

Published
2001
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5. Genome sequence of the pea aphid Acyrthosiphon pisum

Author

Richards, S, Gibbs, RA, Gerardo, NM, Moran, N, Nakabachi, A, Stern, D, Tagu, D, Wilson, ACC, Muzny, D, Kovar, C, Cree, A, Chacko, J, Chandrabose, MN, Dao, MD, Dinh, HH, Gabisi, RA, Hines, S, Hume, J, Jhangian, SN, Joshi, V, Lewis, LR, Liu, Y-S, 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, L-L, Bell, SN, Johnson, AJ, Vattathil, S, Jr, WRL, Shigenobu, S, Dang, PM, Morioka, M, Fukatsu, T, Kudo, T, Miyagishima, S-Y, Jiang, H, Worley, KC, Legeai, F, Gauthier, J-P, Collin, O, Zhang, L, Chen, H-C, Ermolaeva, O, Hlavina, W, Kapustin, Y, Kiryutin, B, Kitts, P, Maglott, D, Murphy, T, Pruitt, K, Sapojnikov, V, Souvorov, A, Thibaud-Nissen, F, Camara, F, Guigo, R, Stanke, M, Solovyev, V, Kosarev, P, Gilbert, D, Gabaldon, 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, Ghanim, M, Heddi, A, Kaloshian, I, Vincent-Monegat, C, Parker, BJ, Perez-Brocal, V, Rahbe, Y, Spragg, CJ, Tamames, J, Tamarit, D, Tamborindeguy, C, Vilcinskas, A, Bickel, RD, Brisson, JA, Butts, T, Chang, C-C, Christiaens, O, Davis, GK, Duncan, E, Ferrier, D, Iga, M, Janssen, R, Lu, H-L, McGregor, A, Miura, T, Smagghe, G, Smith, J, van der Zee, M, Velarde, R, Wilson, M, Dearden, P, Edwards, OR, Gordon, K, Hilgarth, RS, Jr, RSD, Srinivasan, D, Walsh, TK, Ishikawa, A, Jaubert-Possamai, S, Fenton, B, Huang, W, Rizk, G, Lavenier, D, Nicolas, J, Smadja, C, Zhou, J-J, Vieira, FG, He, X-L, Liu, R, Rozas, J, Field, LM, Ashton, PD, Campbell, P, Carolan, JC, Douglas, AE, Fitzroy, CIJ, Reardon, KT, Reeck, GR, 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, CJP, Price, DRG, Caillaud, M, van Fleet, E, Ren, Q, Gatehouse, JA, Brault, V, Monsion, B, Diaz, J, Hunnicutt, L, Ju, H-J, Pechuan, X, Aguilar, J, Cortes, T, Ortiz-Rivas, B, Martinez-Torres, D, Dombrovsky, A, Dale, RP, Davies, TGE, Williamson, MS, Jones, A, Sattelle, D, Williamson, S, Wolstenholme, A, Cottret, L, Sagot, MF, Heckel, DG, Hunter, W, Consortium, IAG, Universitat de Barcelona, Princeton University, Biologie des organismes et des populations appliquées à la protection des plantes (BIO3P), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, Biologie Fonctionnelle, Insectes et Interactions (BF2I), Institut National de la Recherche Agronomique (INRA)-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA), Baylor College of Medicine (BCM), Baylor University, An algorithmic view on genomes, cells, and environments (BAMBOO), Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), IAGC, Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Institut National des Sciences Appliquées (INSA)-Université de Lyon-Institut National des Sciences Appliquées (INSA)-Université de Lyon, Eisen, Jonathan A., and Eisen, Jonathan A

Subjects
0106 biological sciences, TANDEM REPEATS, Genome, Insect, Gene Transfer, RRES175, Sequència genòmica, Faculty of Science\Computer Science, CPG METHYLATION, 01 natural sciences, Genome, Medical and Health Sciences, International Aphid Genomics Consortium, Biologiska vetenskaper, Biology (General), GENE-EXPRESSION, 2. Zero hunger, Genetics, 0303 health sciences, Aphid, Afídids, General Neuroscience, GENOME SEQUENCE, food and beverages, DROSOPHILA CIRCADIAN CLOCK, Biological Sciences, Genetics and Genomics/Microbial Evolution and Genomics, INSECTE, Genètica microbiana, puceron, APIS-MELLIFERA, General Agricultural and Biological Sciences, Infection, symbiose, Biotechnology, Research Article, VIRUS VECTORING, 175_Genetics, SYMBIOTIC BACTERIA, Gene Transfer, Horizontal, QH301-705.5, ACYRTHOSIPHON PISUM, Biology, HOLOMETABOLOUS INSECTS, HOST-PLANT, 010603 evolutionary biology, PEA APHID, INSECT-PLANT, PHENOTYPIC PLASTICITY, RAVAGEUR DES CULTURES, SOCIAL INSECT, General Biochemistry, Genetics and Molecular Biology, Horizontal, 03 medical and health sciences, Buchnera, Gene family, Life Science, Animals, Symbiosis, Gene, 030304 developmental biology, Whole genome sequencing, General Immunology and Microbiology, Annotation, Genome sequence, Agricultural and Veterinary Sciences, 175_Entomology, Genètica animal, Bacteriocyte, génome, gène, Human Genome, Biology and Life Sciences, 15. Life on land, biochemical phenomena, metabolism, and nutrition, biology.organism_classification, REPETITIVE ELEMENTS, DNA-SEQUENCES, Acyrthosiphon pisum, Genome Sequence, Genetics and Genomics/Genome Projects, Aphids, PHEROMONE-BINDING, Insect, Developmental Biology, [SDV.EE.IEO]Life Sciences [q-bio]/Ecology, environment/Symbiosis
Abstract

The genome of the pea aphid shows remarkable levels of gene duplication and equally remarkable gene absences that shed light on aspects of aphid biology, most especially its symbiosis with Buchnera., 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.

Published
2010
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