Acyrthosiphon pisum

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Acyrthosiphon pisum
Acyrthosiphon pisum (pea aphid)-PLoS.jpg
Adult parthenogenetic pea aphid and progeny feeding on a pea plant
Scientific classification OOjs UI icon edit-ltr.svg
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hemiptera
Suborder: Sternorrhyncha
Family: Aphididae
Genus: Acyrthosiphon
Species:
A. pisum
Binomial name
Acyrthosiphon pisum
Harris, 1776
Subspecies
  • A. pisum pisum(type)
  • A. pisum ononisKoch, 1855
  •  ?A. pisum spartiiKoch, 1855
  •  ?A. pisum destructorJohnson, 1900

Acyrthosiphon pisum, commonly known as the pea aphid (and colloquially known as the green dolphin, [1] [2] pea louse, and clover louse [3] ), is a sap-sucking insect in the family Aphididae. It feeds on several species of legumes (plant family Fabaceae) worldwide, including forage crops, such as pea, clover, alfalfa, and broad bean, [4] and ranks among the aphid species of major agronomical importance. [5] The pea aphid is a model organism for biological study whose genome has been sequenced and annotated. [6]

Contents

Generalities and life cycle

In the autumn, female pea aphids lay fertilized eggs overwinter that hatch the following spring. The nymphs that hatch from these eggs are all females, which undergo four moults before reaching sexual maturity. They will then begin to reproduce by viviparous parthenogenesis, like most aphids. Each adult female gives birth to four to 12 female nymphs per day, around a hundred in her lifetime. These develop into mature females in about seven to ten days. The life span of an adult is about 30 days.[ citation needed ]

Population densities are at their highest in early summer, then decrease through predation and parasitism. In autumn, the lengthening of the night triggers the production of a single generation of sexual individuals (males and oviparous females) by the same parthenogenetic parent females. Inseminated sexual females will lay overwintering eggs, from which new parthenogenetic females will emerge in early spring.[ citation needed ]

When the colony begins to become overcrowded, some winged females are produced. These disperse to infest other plants, where they continue to reproduce asexually. When temperatures become colder and day lengths shorter, sexual winged females and males appear. These mate, the females lay diapausing eggs and the life cycle starts again. [7] Pea aphids can complete their whole reproductive cycle without shifting host plant. [8]

Inbreeding is avoided by the recognition of close kin [9] . Mating between close kin has significantly lower egg hatching success and offspring survival than outbred mating [9] .

Several morphs exist in pea aphids. Besides differences between sexual and parthenogenetic morphs, winged and wingless morphs exist. Overcrowding and poor food quality may trigger the development of winged individuals in subsequent generations. [10] Winged aphids can then colonize other host plants. Pea aphids also show hereditary body color variations of green or red/pink. The green morphs are generally more frequent in natural populations. [8]

Acyrthosiphon pisum is a rather large aphid whose body can reach 4 millimetres (5⁄32 in) in adults. [8] It generally feeds on the lower sides of leaves, buds and pods of legumes, ingesting phloem sap through its stylets. Unlike many aphid species, pea aphids do not tend to form dense colonies where individuals would stay where they were born during their whole lifetimes. Pea aphids are not known to be farmed by ants that feed on honeydews.

More than 20 legume genera are known to host pea aphids, though the complete host range remains undetermined. On crops such as peas and alfalfa, A. pisum is considered among the aphid species of major agronomical importance. [5] Yields can be affected by the sap intake that directly weakens plants, although pea aphids seldom reach densities that might significantly reduce crop production. However, like many aphid species, A. pisum can be a vector of viral diseases to the plants it visits. Protection against pea aphids includes the use of chemical insecticides, natural predators and parasitoids, and the selection of resistant cultivars. No insecticide resistance is documented in A. pisum, as opposed to many aphid pests.

Pea aphids, although collectively designated by the single scientific name A. pisum, encompass several biotypes described as cryptic species, subspecies or races, which are specialized on different host species. Therefore, the pea aphid is more accurately described as a species complex. [8]

The pea aphid is thought to be of Palearctic origin, but it is now commonly found worldwide under temperate climate. The spread of A. pisum probably resulted from the introduction of some of its host plants for agriculture. Such an introduction likely occurred into North America during the 1870s, [11] and by 1900 it had become a serious pest species in the mid-Atlantic states. By the 1950s, it was widespread throughout the United States and Canada. Its host range in North America is very similar to that of the closely related blue alfalfa aphid (Acyrthosiphon kondoi). [12]

Model organism

Adult, parthenogentic pea aphid on alfalfa - this red morph shows the reddish/dark markings due to carotenoids that some individuals produce. Peaaphidafalfa.jpg
Adult, parthenogentic pea aphid on alfalfa - this red morph shows the reddish/dark markings due to carotenoids that some individuals produce.

A. pisum is considered as the model aphid species. Its reproductive cycle, including the sexual phase and the overwintering of eggs, can be easily completed on host plants under laboratory conditions, and the relatively large size of individuals facilitates physiological studies. In 2010, the International Aphid Genomics Consortium published an annotated draft sequence of the pea aphid genome [6] composed of approximately 525 megabases and 34000 predicted genes in 2n=8 chromosomes. This constitutes the first genome of a hemimetabolous [13] insect to have been published. The pea aphid genome and other of its features are the focus of studies covering the following areas:

Endosymbiotic relationship with Buchnera aphidicola

A. pisum participates in an obligate endosymbiotic relationship with the bacteria Buchnera aphidicola. A. pisum is the host and Buchnera is the primary endosymbiont. Together they form the holosymbiont. [23] This is an obligate, symbiotic relationship and both partners are completely dependent on each other. [23] [24] When treated with antibiotics to remove the Buchnera bacteria, A. pisum growth and reproduction are interrupted or reduced. Buchnera lacks genes required for living independent of a host and is unculturable outside of the aphid host. [25] The A. pisum and Buchnera holosymbiont is one of the most well studied symbiotic relationships both genetically and experimentally.

Evolution of the endosymbiotic relationship

The A. pisum and Buchnera endosymbiotic relationship is likely to have evolved 160-280 million years ago. Phylogenetic analysis shows that Buchnera is a monophyletic group and that the phylogenies of Buchnera and A. pisum coincide. Therefore, there was likely one original Buchnera infection of the common ancestor of aphids and co-speciation of the holosymbiont has occurred since then. [26] Buchnera is related to Enterobacteriaceae including Escheriachia coli [24] and it is likely that Buchnera evolved from a bacterium that originally occupied the gut of the aphid common ancestor. [27]

Nutritional symbiosis

Like other insects of the order Hemiptera, A.pisum utilizes an endosymbiotic bacterium to overcome the nutritional deficiencies of phloem sap. [23] [28] A. pisum feeds on phloem sap of host plants including Medicago sativa (alfalfa), Pisum sativa (pea), Trifolium pretense (red clover), and Vicia faba (broad bean). The phloem saps of these plants are nutritionally rich in carbohydrates but poor in terms of nitrogen. [29] [30] [31] [32] The ratio of essential amino acids to nonessential amino acids in these phloem saps ranges from 1:4-1:20. This ratio of essential to nonessential amino acids is severely disproportional compared to the 1:1 ratio present in animal tissues and necessary for survival. [30] Animals, including A. pisum, can produce nonessential amino acids de novo but cannot synthesize nine essential amino acids that must be obtained through their diets: histidine, isoleucine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine. In addition to these nine essential amino acids, A. pisum is unable to synthesize arginine due to missing urea cycle genes. [23] [33] [34] The endosymbiotic relationship with Buchnera allows A. pisum to overcome this lack of essential amino acids in the phloem sap [24] [30] [31] [34] [35] When provided with nonessential amino acids, Buchnera converts nonessential amino acids into essential amino acids to be returned to A. pisum. [28] [36] This nutritional provisioning has been examined genomically (metabolic complementary, discussed below) and experimentally. Isolated bacteriocytes containing Buchnera have been shown to actively take up 14C labeled glutamine (a nonessential amino acid) where it is then converted into glutamic acid. [36] This glutamic acid is then taken up by the individual Buchnera cells and used to synthesize the essential amino acids isoleucine, leucine, phenylalanine, and valine as well as nonessential amino acids that can be returned to A. pisum. Mutual nutrient provisioning is likely the main reason for the persistence of this symbiosis. [34]

Holosymbiont structure

Buchnera are housed in specialized, aphid-derived cells located in the hemocoel of the A. pisum body cavity. [23] [24] Each Buchnera cell has an inner and outer gram-negative cell membrane and is individually enclosed in an aphid-derived symbiosomal membrane. These encased cells are then grouped into specialized, aphid-derived bacteriocytes (mycetocytes). Bacteriocytes are large, polyploid cells surrounded by a thin lining of flat sheath cells. There are about 60-80 bacteriocytes in each pea aphid and are organized into the bi-lobed bacteriome. A bacteriome is a specialized organ that runs along the length of the pea aphid on two sides of the body and joins near the hindgut. [24] [33] [37] Bacteriocytes are located near the ovariole cluster and Buchnera cells are vertically transferred from the mother's ovaries through transovarial transmission. [24] [27] The Buchnera cells are transferred to eggs during oogenesis or to the developing embryos during embryogenesis. [23]

Genome sequencing

A. pisum and Buchnera were the first insect-endosymbiont pair to have the genomes of both partners sequenced. [38] This has provided researchers with a great deal of information about the evolutionary and molecular interactions of this endosymbiosis. [33] The A. pisum and Buchnera genomes have experienced unique modifications that are likely related to the establishment and maintenance of the endosymbiotic relationship. The genomes of both organisms have undergone significant gene loss compared to related organisms. The Buchnera genome is 641-kb and consists of a circular chromosome with 2 plasmids. It has been reduced to one-seventh of the size of its closest free-living relative, E. coli. [25] [33] Buchnera has lost genes that would allow it to live outside the host but maintains genes essential for the nutrition of A. pisum. [23] [24] [25] [33] [34] The Buchnera genome is missing genes required for surface membrane construction such as lipopolysaccharides and phospholipids as well as genes associated with cellular defense. Transporter genes and regulatory genes are also missing from the genome. Such gene loss is typical of an obligate and intracellular bacterium. [25] [34]

The A. pisum genome has undergone more unique genomic changes compared to other insects of the order Hemiptera. The aphid genome is 464MB with aphid-specific orphan genes making up 20% of the genome and gene duplication present in more than 2000 gene families. [23] [34] These orphan genes and gene duplications are likely associated with the “metabolic, structural and developmental” components of the endosymbiotic relationship. [34] A. pisum specific gene duplications of amino acid transporters highly expressed in bacteriocytes have been observed. [39] These duplications are likely associated with the genetic establishment and maintenance of the endosymbiotic relationship.

No lateral gene transfer has been detected between A. pisum and Buchnera. It was previously believed that lateral gene transfer was responsible for the severe gene reduction in the Buchnera genome but sequencing has shown that this has not occurred. [25] [34]

Metabolic complementarity

Individually, the metabolic pathways of A. pisum and Buchnera are incomplete. Jointly, the genomes of these two organisms complement each other to produce complete metabolic pathways for the biosynthesis of nutrients such as amino acids and other essential molecules. [23] [33] [34] [40] The ancestral partners of this symbiosis are likely to have had complete metabolic pathways, however pressure to maintain these pathway genes was reduced due to redundancy as a result of the presence of the other partner's genome. [40] Unlike other related insects, the A. pisum genome is missing genes necessary for the urea cycle. [23] [33] [37] the purine salvage pathway, [40] and other genes that code enzymes necessary for the biosynthesis of molecules. [33] [34] These missing reaction intermediates are likely provided by genes within the Buchnera genome. For example, A. pisum is the only species with a sequenced genome known to be missing key components of the purine salvage pathway, essential for the production of DNA, RNA, signaling molecules, and ATP. The Buchnera genome contains the necessary genes to encode the reaction intermediates missing from the A. pisum genome. Through this complementation, the nucleotide requirements of both organisms are fulfilled: the purine salvage pathway is completed for A. pisum and Buchnera receives necessary guanosine. [40]

The Buchnera genome has retained genes required for the biosynthesis of essential amino acids but has not retained genes responsible for the degradation of amino acids. The A. pisum genome on the other hand, contains 66 amino acid biosynthesis genes and 93 amino acid degradation genes. [23] [33] Both A. pisum and Buchnera contribute to the metabolic pathways of amino acid biosynthesis. [23] [33] [34] This metabolic complementarity is illustrated by the use of asparagine, a nonessential amino acid in phloem sap, as a major precursor in the production essential and nonessential amino acids necessary for the growth and survival of A. pisum and Buchnera. [34]

Immune system

Genome sequencing of A. pisum shows that the genome lacks expected genes essential to immune response pathways. [13] The A. pisum genome lacks IMS, dFADD, Dredd and Retish genes that are a part of the IMD (immunodeficiency) pathway and present in other related insects. Also missing are peptidoglycan recognition proteins (PGRPs) that detect pathogens and alert the IMD pathway as well as antimicrobial peptide (AMP) genes which are produced once the immune pathway has been activated. A reduced immune system may have facilitated the establishment and sustained maintenance of the symbiotic relationship between the Buchnera bacterium and A. pisum. [23] [34] Also, phloem sap is a diet with reduced amounts of microbes which may have lower the evolutionary pressure of A. pisum to maintain the immune response pathway genes. [34] [13]

Pests, diseases, and biocontrols

A. pisum faces threats from parasitoid wasps and the fungal pathogen Pandora neoaphidis . As such these are also promising potential biocontrols. [13]

Related Research Articles

<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is any organism that lives within the body or cells of another organism most often, though not always, in a mutualistic relationship. (The term endosymbiosis is from the Greek: ἔνδον endon "within", σύν syn "together" and βίωσις biosis "living".) Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals and bacterial endosymbionts that provide essential nutrients to insects.

<span class="mw-page-title-main">Aphid</span> Superfamily of insects

Aphids are small sap-sucking insects and members of the superfamily Aphidoidea. Common names include greenfly and blackfly, although individuals within a species can vary widely in color. The group includes the fluffy white woolly aphids. A typical life cycle involves flightless females giving live birth to female nymphs—who may also be already pregnant, an adaptation scientists call telescoping generations—without the involvement of males. Maturing rapidly, females breed profusely so that the number of these insects multiplies quickly. Winged females may develop later in the season, allowing the insects to colonize new plants. In temperate regions, a phase of sexual reproduction occurs in the autumn, with the insects often overwintering as eggs.

<span class="mw-page-title-main">Sap</span> Fluid transported in xylem cells or phloem sieve tube elements of a plant

Sap is a fluid transported in xylem cells or phloem sieve tube elements of a plant. These cells transport water and nutrients throughout the plant.

<span class="mw-page-title-main">Aphididae</span> Family of true bugs

The Aphididae are a very large insect family in the aphid superfamily (Aphidoidea), of the order Hemiptera. These insects suck the sap from plant leaves. Several thousand species are placed in this family, many of which are considered plant/crop pests. They are the family of insects containing most plant virus vectors with the green peach aphid being one of the most prevalent and indiscriminate carriers.

A bacteriome is a specialized organ, found mainly in some insects, that hosts endosymbiotic bacteria. Bacteriomes contain specialized cells, called bacteriocytes, that provide nutrients and shelter to the bacteria while protecting the host animal. In exchange, the bacteria provide essentials like vitamins and amino acids to the host insect. Bacteriomes also protect the bacteria from the host's immune system, with insects secreting antimicrobial peptides such as the coleoptericin secreted by weevils to keep bacteria within the bacteriome.

<span class="mw-page-title-main">Genome size</span> Amount of DNA contained in a genome

Genome size is the total amount of DNA contained within one copy of a single complete genome. It is typically measured in terms of mass in picograms or less frequently in daltons, or as the total number of nucleotide base pairs, usually in megabases. One picogram is equal to 978 megabases. In diploid organisms, genome size is often used interchangeably with the term C-value.

<i>Buchnera aphidicola</i> Species of bacterium

Buchnera aphidicola, a member of the Pseudomonadota and the only species in the genus Buchnera, is the primary endosymbiont of aphids, and has been studied in the pea aphid, Acyrthosiphon pisum. Buchnera is believed to have had a free-living, Gram-negative ancestor similar to a modern Enterobacterales, such as Escherichia coli. Buchnera is 3 µm in diameter and has some of the key characteristics of their Enterobacterales relatives, such as a Gram-negative cell wall. However, unlike most other Gram-negative bacteria, Buchnera lacks the genes to produce lipopolysaccharides for its outer membrane. The long association with aphids and the limitation of crossover events due to strictly vertical transmission has seen the deletion of genes required for anaerobic respiration, the synthesis of amino sugars, fatty acids, phospholipids, and complex carbohydrates. This has resulted not only in one of the smallest known genomes of any living organism, but also one of the most genetically stable.

<span class="mw-page-title-main">Bacteriocyte</span>

A bacteriocyte, also known as a mycetocyte, is a specialized adipocyte found primarily in certain insect groups such as aphids, tsetse flies, German cockroaches, weevils. These cells contain endosymbiotic organisms such as bacteria and fungi, which provide essential amino acids and other chemicals to their host. Bacteriocytes may aggregate into a specialized organ called the bacteriome.

"Candidatus Carsonella ruddii" is an obligate endosymbiotic Gammaproteobacterium with one of the smallest genomes of any characterised bacteria.

Nancy A. Moran is an American evolutionary biologist and entomologist, University of Texas Leslie Surginer Endowed Professor, and co-founder of the Yale Microbial Diversity Institute. Since 2005, she has been a member of the United States National Academy of Sciences. Her seminal research has focused on the pea aphid, Acyrthosiphon pisum and its bacterial symbionts including Buchnera (bacterium). In 2013, she returned to the University of Texas at Austin, where she continues to conduct research on bacterial symbionts in aphids, bees, and other insect species. She has also expanded the scale of her research to bacterial evolution as a whole. She believes that a good understanding of genetic drift and random chance could prevent misunderstandings surrounding evolution. Her current research goal focuses on complexity in life-histories and symbiosis between hosts and microbes, including the microbiota of insects.

The hologenome theory of evolution recasts the individual animal or plant as a community or a "holobiont" – the host plus all of its symbiotic microbes. Consequently, the collective genomes of the holobiont form a "hologenome". Holobionts and hologenomes are structural entities that replace misnomers in the context of host-microbiota symbioses such as superorganism, organ, and metagenome. Variation in the hologenome may encode phenotypic plasticity of the holobiont and can be subject to evolutionary changes caused by selection and drift, if portions of the hologenome are transmitted between generations with reasonable fidelity. One of the important outcomes of recasting the individual as a holobiont subject to evolutionary forces is that genetic variation in the hologenome can be brought about by changes in the host genome and also by changes in the microbiome, including new acquisitions of microbes, horizontal gene transfers, and changes in microbial abundance within hosts. Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts. For recent literature on holobionts and hologenomes published in an open access platform, see the following reference.

The minimal genome is a concept which can be defined as the set of genes sufficient for life to exist and propagate under nutrient-rich and stress-free conditions. Alternatively, it can also be defined as the gene set supporting life on an axenic cell culture in rich media, and it is thought what makes up the minimal genome will depend on the environmental conditions that the organism inhabits. By one early investigation, the minimal genome of a bacterium should include a virtually complete set of proteins for replication and translation, a transcription apparatus including four subunits of RNA polymerase including the sigma factor rudimentary proteins sufficient for recombination and repair, several chaperone proteins, the capacity for anaerobic metabolism through glycolysis and substrate-level phosphorylation, transamination of glutamyl-tRNA to glutaminyl-tRNA, lipid biosynthesis, eight cofactor enzymes, protein export machinery, and a limited metabolite transport network including membrane ATPases. Proteins involved in the minimum bacterial genome tend to be substantially more related to proteins found in archaea and eukaryotes compared to the average gene in the bacterial genome more generally indicating a substantial number of universally conserved proteins. The minimal genomes reconstructed on the basis of existing genes does not preclude simpler systems in more primitive cells, such as an RNA world genome which does not have the need for DNA replication machinery, which is otherwise part of the minimal genome of current cells.

Hamiltonella defensa is a species of bacteria. It is maternally or sexually transmitted and lives as an endosymbiont of whiteflies and aphids, meaning that it lives within a host, protecting its host from attack. It does this through bypassing the host's immune responses by protecting its host against parasitoid wasps. However, H. defensa is only defensive if infected by a virus. H. defensa shows a relationship with Photorhabdus species, together with Regiella insecticola. Together with other endosymbionts, it provides aphids protection against parasitoids. It is known to habitate Bemisia tabaci.

Arsenophonus nasoniae is a species of bacterium which was previously isolated from Nasonia vitripennis, a species of parasitoid wasp. These wasps are generalists which afflict the larvae of parasitic carrion flies such as blowflies, houseflies and flesh flies. A. nasoniae belongs to the phylum Pseudomonadota and family Morganellaceae.The genus Arsenophonus, has a close relationship to the Proteus (bacterium) rather than to that of Salmonella and Escherichia. The genus is composed of gammaproteobacterial, secondary-endosymbionts which are gram-negative. Cells are non-flagellated, non-motile, non-spore forming and form long to highly filamentous rods. Cellular division is exhibited through septation. The name 'Arsenophonus nasoniae gen. nov., sp. nov.' was therefore proposed for the discovered bacterium due to its characteristics and its microbial interaction with N. vitripennis. The type strain of A. nasoniae is Strain SKI4.

Nasuia deltocephalinicola was reported in 2013 to have the smallest genome of all bacteria, with 112,091 nucleotides. For comparison, the human genome has 3.2 billion nucleotides. The second smallest genome, from bacteria Tremblaya princeps, has 139,000 nucleotides. While N. deltocephalinicola has the smallest number of nucleotides, it has more protein-coding genes (137) than some bacteria.

"Candidatus Karelsulcia muelleri" is an aerobic, gram-negative, bacillus bacterium that is a part of the phylum Bacteroidota. "Ca. K. muelleri" is an obligate and mutualistic symbiotic microbe commonly found occupying specialized cell compartments of sap-feeding insects called bacteriocytes. A majority of the research done on "Ca. K. muelleri" has detailed its relationship with the host Homalodisca vitripennis. Other studies have documented the nature of its residency in other insects like the maize leafhopper (Cicadulina) or the spittlebug (Cercopoidea). "Ca. K. muelleri" is noted for its exceptionally minimal genome and it is currently identified as having the smallest known sequenced Bacteroidota genome at only 245 kilobases.

Angela Elizabeth Douglas is a British entomologist who researches insect nutrition, and is known for her research on symbiotic relationships between insects and microorganisms. She has been the Daljit S. and Elaine Sarkaria Professor of Insect Physiology and Toxicology at Cornell University, Ithaca, New York, since 2008, and previously held a chair at the University of York (2003–8).

<span class="mw-page-title-main">Imd pathway</span> Immune signaling pathway of insects

The Imd pathway is a broadly-conserved NF-κB immune signalling pathway of insects and some arthropods that regulates a potent antibacterial defence response. The pathway is named after the discovery of a mutation causing severe immune deficiency. The Imd pathway was first discovered in 1995 using Drosophila fruit flies by Bruno Lemaitre and colleagues, who also later discovered that the Drosophila Toll gene regulated defence against Gram-positive bacteria and fungi. Together the Toll and Imd pathways have formed a paradigm of insect immune signalling; as of September 2, 2019, these two landmark discovery papers have been cited collectively over 5000 times since publication on Google Scholar.

Vertical transmission of symbionts is the transfer of a microbial symbiont from the parent directly to the offspring. Many metazoan species carry symbiotic bacteria which play a mutualistic, commensal, or parasitic role. A symbiont is acquired by a host via horizontal, vertical, or mixed transmission.

Reductive evolution is the process by which microorganisms remove genes from their genome. It can occur when bacteria found in a free-living state enter a restrictive state or are completely absorbed by another organism becoming intracellular (symbiogenesis). The bacteria will adapt to survive and thrive in the restrictive state by altering and reducing its genome to get rid of the newly redundant pathways that are provided by the host. In an endosymbiont or symbiogenesis relationship where both the guest and host benefit, the host can also undergo reductive evolution to eliminate pathways that are more efficiently provided for by the guest.

References

  1. ↑ Cyrus, Thomas (1879). "Noxious and beneficial insects of the state of Illinois". Report of the State Entomologist (Illinois). 8: 1–212.
  2. ↑ Davis, John (1915). The pea aphis with relation to forage crops (276 ed.). US Department of Agriculture.
  3. ↑ Folsom, Justus W. (1909). The insect pests of clover and alfalfa (134 ed.). Urbana, Illinois, USA: University of Illinois Agricultural Experiment Station. pp.  138–154. pea aphid green dolphin.
  4. ↑ "Acyrthosiphon pisum". AphID. Retrieved 19 March 2013. It is particularly important on peas, beans, alfalfa and clover, but also attacks beets, cucurbits, various species of Brassicaceae. It has been implicated in the transmission of over 40 plant viruses.
  5. 1 2 van Emden, H. & Harrington, R. Aphids As Crop Pests. (CABI, 2007).
  6. 1 2 3 The International Aphid Genomics Consortium (2010). "Genome Sequence of the Pea Aphid Acyrthosiphon pisum". PLOS Biology. 8 (2): e1000313. doi:10.1371/journal.pbio.1000313. PMC   2826372 . PMID   20186266.
  7. ↑ Dixon, A. F. G. Aphid Ecology - An optimization approach. 2 edn, (Kluwer Academic Pub, 1998).
  8. 1 2 3 4 Eastop, V. F. Keys for the identification of Acyrthosiphon (Hemiptera : Aphididae). Bulletin of the British Museum (Natural History) Entomology 26 (1971).
  9. 1 2 Huang MH, Caillaud MC. Inbreeding avoidance by recognition of close kin in the pea aphid, Acyrthosiphon pisum. J Insect Sci. 2012;12:39. doi: 10.1673/031.012.3901. PMID: 22954315; PMCID: PMC3471804
  10. 1 2 Braendle, C.; Davis, G. K.; Brisson, J. A.; Stern, D. L. (2006). "Wing dimorphism in aphids". Heredity. 97 (3): 192–9. doi: 10.1038/sj.hdy.6800863 . PMID   16823401.
  11. ↑ Thomas, C. A list of the species of the tribe Aphidini, family Aphidae, found in the United States, which have been heretofore named with descriptions of some new species. Bull. Illinois State Lab. Natural History 2, 3-16 (1878).
  12. ↑ Capinera, John L. (2001). Handbook of Vegetable Pests. Gulf Professional Publishing. pp. 317–320. ISBN   978-0-12-158861-8.
  13. 1 2 3 4 5 6 7 Gerardo, Nicole M; Altincicek, Boran; Anselme, Caroline; Atamian, Hagop; Barribeau, Seth M; de Vos, Martin; Duncan, Elizabeth J; Evans, Jay D; Gabaldón, Toni; Ghanim, Murad; Heddi, Adelaziz; Kaloshian, Isgouhi; Latorre, Amparo; Moya, Andres; Nakabachi, Atsushi; Parker, Benjamin J; Pérez-Brocal, Vincente; Pignatelli, Miguel; Rahbé, Yvan; Ramsey, John S; Spragg, Chelsea J; Tamames, Javier; Tamarit, Daniel; Tamborindeguy, Cecilia; Vincent-Monegat, Caroline; Vilcinskas, Andreas (2010). "Immunity and other defenses in pea aphids, Acyrthosiphon pisum". Genome Biology . BioMed Central. 11 (2): R21. doi:10.1186/gb-2010-11-2-r21. PMC   2872881 . PMID   20178569. S2CID   5249535.
  14. ↑ Tsuchida, T.; Koga, R.; Horikawa, M.; Tsunoda, T.; Maoka, T.; Matsumoto, S.; Simon, J. -C.; Fukatsu, T. (2010). "Symbiotic Bacterium Modifies Aphid Body Color". Science. 330 (6007): 1102–4. Bibcode:2010Sci...330.1102T. doi:10.1126/science.1195463. PMID   21097935. S2CID   206529034.
  15. ↑ Scarborough, C. L.; Ferrari, J.; Godfray, H. (2005). "Aphid Protected from Pathogen by Endosymbiont". Science. 310 (5755): 1781. doi:10.1126/science.1120180. PMID   16357252. S2CID   32543175.
  16. ↑ Tsuchida, T.; Koga, R.; Fukatsu, T. (2004). "Host Plant Specialization Governed by Facultative Symbiont". Science. 303 (5666): 1989. doi:10.1126/science.1094611. PMID   15044797. S2CID   46139967.
  17. 1 2 Simon, J. C.; Stoeckel, S.; Tagu, D. (2010). "Evolutionary and functional insights into reproductive strategies of aphids". Comptes Rendus Biologies. 333 (6–7): 488–96. doi:10.1016/j.crvi.2010.03.003. PMID   20541160.
  18. ↑ Brisson, J. A.; Nuzhdin, S. V. (2008). "Rarity of Males in Pea Aphids Results in Mutational Decay". Science. 319 (5859): 58. Bibcode:2008Sci...319...58B. doi:10.1126/science.1147919. PMID   18174433. S2CID   34320106.
  19. ↑ Nancy A. Moran; Tyler Jarvik (2010). "Lateral Transfer of Genes from Fungi Underlies Carotenoid Production in Aphids". Science. 328 (5978): 624–627. Bibcode:2010Sci...328..624M. doi:10.1126/science.1187113. PMID   20431015. S2CID   14785276.
  20. ↑ Hawthorne, D. J.; Via, S. (2001). "Genetic linkage of ecological specialization and reproductive isolation in pea aphids". Nature. 412 (6850): 904–7. Bibcode:2001Natur.412..904H. doi:10.1038/35091062. PMID   11528477. S2CID   4325260.
  21. ↑ Mutti, N. S.; Louis, J.; Pappan, L. K.; Pappan, K.; Begum, K.; Chen, M. -S.; Park, Y.; Dittmer, N.; Marshall, J.; Reese, J. C.; Reeck, G. R. (2008). "A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant". Proceedings of the National Academy of Sciences. 105 (29): 9965–9. Bibcode:2008PNAS..105.9965M. doi: 10.1073/pnas.0708958105 . PMC   2481341 . PMID   18621720.
  22. ↑ Peccoud, J.; Simon, J.-C. (2010). "The pea aphid complex as a model of ecological speciation". Ecological Entomology. 35: 119–130. doi: 10.1111/j.1365-2311.2009.01147.x .
  23. 1 2 3 4 5 6 7 8 9 10 11 12 13 IAGC (2010) Genome Sequence of the Pea Aphid Acyrthosiphon pisum. Plos Biol 8
  24. 1 2 3 4 5 6 7 Brinza, L., et al. (2009) Systemic analysis of the symbiotic function of Buchnera aphidicola, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. Cr Biol 332, 1034-1049
  25. 1 2 3 4 5 Shigenobu, S.; et al. (2000). "Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS". Nature. 407 (6800): 81–86. Bibcode:2000Natur.407...81S. doi: 10.1038/35024074 . PMID   10993077.
  26. ↑ oran, N.A., et al. (1993) A Molecular Clock in Endosymbiotic Bacteria is Calibrated Using the Insect Hosts. Proceedings of the Royal Society of London. Series B: Biological Sciences 253, 167-171
  27. 1 2 Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43, 17-37
  28. 1 2 Baumann, P.; et al. (1995). "Genetics, Physiology, and Evolutionary Relationships of the Genus Buchnera - Intracellular Symbionts of Aphids". Annu Rev Microbiol. 49: 55–94. doi:10.1146/annurev.micro.49.1.55. PMID   8561471.
  29. ↑ Douglas, A.E. (1993) The Nutritional Quality of Phloem Sap Utilized by Natural Aphid Populations. Ecol Entomol 18, 31-38
  30. 1 2 3 Douglas, A.E. (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57, 747-754
  31. 1 2 Gunduz, E.A. and Douglas, A.E. (2009) Symbiotic bacteria enable insect to use a nutritionally inadequate diet. P Roy Soc B-Biol Sci 276, 987-991
  32. ↑ Sandstrom, J. and Moran, N. (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol Exp Appl 91, 203-210
  33. 1 2 3 4 5 6 7 8 9 10 Wilson, A.C.C., et al. (2010) Genomic insight into the amino acid relations of the pea aphid, Acyrthosiphon pisum, with its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19, 249-258
  34. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Shigenobu, S.; Wilson, A.C.C. (2011). "Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont". Cell Mol Life Sci. 68 (8): 1297–1309. doi:10.1007/s00018-011-0645-2. PMC   3064905 . PMID   21390549.
  35. ↑ Sandstrom, J. and Pettersson, J. (1994) Amino-Acid-Composition of Phloem Sap and the Relation to Intraspecific Variation in Pea Aphid (Acyrthosiphon-Pisum) Performance. J Insect Physiol 40, 947-955
  36. 1 2 Sasaki, T. and Ishikawa, H. (1995) Production of Essential Amino-Acids from Glutamate by Mycetocyte Symbionts of the Pea Aphid, Acyrthosiphon-Pisum. J Insect Physiol 41, 41-46
  37. 1 2 Wilson, A.C.C., et al. (2003) Heritable genetic variation and potential for adaptive evolution in asexual aphids (Aphidoidea). Biol J Linn Soc 79, 115-135
  38. ↑ Gerardo, N.M.; Wilson, A.C.C. (2011). "The power of paired genomes". Mol Ecol. 20 (10): 2038–2040. doi:10.1111/j.1365-294x.2011.05103.x. PMID   21692233. S2CID   20882842.
  39. ↑ Price, D.R.G.; et al. (2011). "Genome Expansion and Differential Expression of Amino Acid Transporters at the Aphid/Buchnera Symbiotic Interface". Mol Biol Evol. 28 (11): 3113–3126. doi: 10.1093/molbev/msr140 . PMID   21613235.
  40. 1 2 3 4 Ramsey, J.S., et al. (2010) Genomic evidence for complementary purine metabolism in the pea aphid, Acyrthosiphon pisum, and its symbiotic bacterium Buchnera aphidicola. Insect Mol Biol 19, 241-248
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