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Integrative Genomic Approaches to Studying Epigenetic Mechanisms of Phenotypic Plasticity in the Aphid

  • Mary Grantham
  • Jennifer A. Brisson
  • Denis Tagu
  • Gael Le TrionnaireEmail author
Chapter
Part of the Entomology in Focus book series (ENFO, volume 3)

Abstract

Phenotypic plasticity is the nongenic variation in phenotype due to environmental factors. It is a common phenomenon in the animal kingdom that is not well understood at the molecular level. A tenable form of phenotypic plasticity for molecular research is polyphenism, which is an extreme form of phenotypic plasticity that results in discrete, alternative morphs. Epigenetic mechanisms have been hypothesized as the molecular regulators of polyphenism, in particular DNA methylation and chromatin remodeling. The pea aphid exhibits multiple polyphenisms including winged and wingless females during summer (wing polyphenism) and asexual and sexual morphs during summer and fall, respectively (reproductive polyphenism). The aphid is ideally situated for research into the molecular basis of polyphenism, with a sequenced genome and multiple transcriptomic studies that have begun identifying key molecular regulators of these two polyphenisms. The aphid also possesses the genes necessary for DNA methylation and chromatin remodeling. The pea aphid system is thus primed for future research into the epigenetic regulation of polyphenisms.

Keywords

Phenotypic Plasticity Juvenile Hormone Cluster Regularly Interspaced Short Palindromic Repeat Royal Jelly Sexual Morph 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ANT

Adenine nucleotide translocase gene

CHiP-seq

Chromatin immunoprecipitation sequencing

CRISPR

Clustered regularly interspaced short palindromic repeat

crRNA

CRISPR transcript

DNase-seq

DNAse I hypersensitive site mapping

DNMT

DNA methyltransferase

FAIRE-seq

Formaldehyde-assisted isolation of regulatory elements

GO

Gene Ontology

H3K4me1

Mono-methylated lysine residue of histone H3

H3K4me2

Di-methylated lysine residue of histone H3

JH

Juvenile hormone

LSD1

Lysine-specific demethylase 1

MethylC-seq

Whole-genome bisulfite sequencing

NBAD

N-β alanyl dopamine

TALE

Transcription activator-like effector

TOL

Takeout-like gene

References

  1. 1.
    West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, Oxford/New YorkGoogle Scholar
  2. 2.
    de Jong M, Leyser O (2012) Developmental plasticity in plants. Cold Spring Harb Symp Quant Biol 77:63–73. doi: 10.1101/sqb.2012.77.014720 CrossRefPubMedGoogle Scholar
  3. 3.
    Aubin-Horth N, Renn SCP (2009) Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity. Mol Ecol 18(18):3763–3780. doi: 10.1111/j.1365-294X.2009.04313.x CrossRefPubMedGoogle Scholar
  4. 4.
    Beldade P, Mateus ARA, Keller RA (2011) Evolution and molecular mechanisms of adaptive developmental plasticity. Mol Ecol 20(7):1347–1363. doi: 10.1111/j.1365-294X.2011.05016.x CrossRefPubMedGoogle Scholar
  5. 5.
    De Loof A, Boerjan B, Ernst UR, Schoofs L (2013) The mode of action of juvenile hormone and ecdysone: towards an epi-endocrinological paradigm? Gen Comp Endocrinol 188:35–45. doi: 10.1016/j.ygcen.2013.02.004 CrossRefPubMedGoogle Scholar
  6. 6.
    Bell O, Tiwari VK, Thoma NH, Schubeler D (2011) Determinants and dynamics of genome accessibility. Nat Rev Genet 12(8):554–564. doi: 10.1038/nrg3017 CrossRefPubMedGoogle Scholar
  7. 7.
    Scheer BT (1961) The neuroendocrine system of arthropods. Vitam Horm 18:141–204. doi: 10.1016/S0083-6729(08)60862-6
  8. 8.
    Tawfik AI (2012) Hormonal control of the phase polyphenism of the desert locust: a review of current understanding. Open Entomol J 6:22–41CrossRefGoogle Scholar
  9. 9.
    Nijhout HF (1999) Control mechanisms of polyphenic development in insects: in polyphenic development, environmental factors alter some aspects of development in an orderly and predictable way. BioScience 49(3):181–192. doi: 10.2307/1313508 CrossRefGoogle Scholar
  10. 10.
    Nijhout HF (1994) Insect hormones. Princeton University Press, PrincetonGoogle Scholar
  11. 11.
    Kucharski R, Maleszka J, Foret S, Maleszka R (2008) Nutritional control of reproductive status in honeybees via DNA methylation. Science 319(5871):1827–1830. doi: 10.1126/science.1153069 CrossRefPubMedGoogle Scholar
  12. 12.
    Foret S, Kucharski R, Pellegrini M, Feng S, Jacobsen SE, Robinson GE, Maleszka R (2012) DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees. Proc Natl Acad Sci U S A 109(13):4968–4973. doi: 10.1073/pnas.1202392109 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Lyko F, Foret S, Kucharski R, Wolf S, Falckenhayn C, Maleszka R (2010) The honey bee epigenomes: differential methylation of brain DNA in queens and workers. PLoS Biol 8(11):e1000506. doi: 10.1371/journal.pbio.1000506 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Spannhoff A, Kim YK, Raynal NJ, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JP, Bedford MT (2011) Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep 12(3):238–243. doi: 10.1038/embor.2011.9 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Simola DF, Ye C, Mutti NS, Dolezal K, Bonasio R, Liebig J, Reinberg D, Berger SL (2013) A chromatin link to caste identity in the carpenter ant Camponotus floridanus. Genome Res 23(3):486–496. doi: 10.1101/gr.148361.112 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Koch PB, Brakefield PM, Kesbeke F (1996) Ecdysteroids control eyespot size and wing color pattern in the polyphenic butterfly Bicyclus anynana (Lepidoptera: Satyridae). J Insect Physiol 42(3):223–230. doi: 10.1016/0022-1910(95)00103-4 CrossRefGoogle Scholar
  17. 17.
    Wolschin F, Mutti NS, Amdam GV (2011) Insulin receptor substrate influences female caste development in honeybees. Biol Lett 7(1):112–115. doi: 10.1098/rsbl.2010.0463 CrossRefPubMedGoogle Scholar
  18. 18.
    Snell-Rood EC, Moczek AP (2012) Insulin signaling as a mechanism underlying developmental plasticity: the role of FOXO in a nutritional polyphenism. PLoS One 7(4):e34857. doi: 10.1371/journal.pone.0034857 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ (2009) Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323(5914):627–630. doi: 10.1126/science.1165939 CrossRefPubMedGoogle Scholar
  20. 20.
    Gilbert LI (2012) Insect endocrinology, 1st edn. Elsevier/Academic, London/WalthamGoogle Scholar
  21. 21.
    Blackman RL, Eastop VF (2000) Aphids on the world’s crops: an identification and information guide, 2nd edn. Wiley, Chichester/New YorkGoogle Scholar
  22. 22.
    Dixon AFG (1974) Biology of aphids. J Entomol Ser A Gen Entomol 48(2):156–156. doi: 10.1111/j.1365-3032.1974.tb00049.x Google Scholar
  23. 23.
    Oerke EC (1994) Crop production and crop protection: estimated losses in major food and cash crops. Elsevier, Amsterdam/New YorkGoogle Scholar
  24. 24.
    Morrison WP, Peairs F (1998) Response model concept and economic impact. Response model for an introduced pest—the Russian wheat aphid. Entomological Society of America, LanhamGoogle Scholar
  25. 25.
    Blackman R (1987) Reproduction, cytogenetics and development. Aphids: their biology, natural enemies, and control. Elsevier Science Publishers, AmsterdamGoogle Scholar
  26. 26.
    Smith MAH, MacKay PA (1989) Genetic variation in male alary dimorphism in populations of pea aphid, Acyrthosiphon pisum. Entomol Exp Appl 51(2):125–132. doi: 10.1111/j.1570-7458.1989.tb01222.x CrossRefGoogle Scholar
  27. 27.
    Braendle C, Caillaud MC, Stern DL (2005) Genetic mapping of aphicarus – a sex-linked locus controlling a wing polymorphism in the pea aphid (Acyrthosiphon pisum). Heredity 94(4):435–442. doi: 10.1038/sj.hdy.6800633 CrossRefPubMedGoogle Scholar
  28. 28.
    Müller CB, Williams IS, Hardie J (2001) The role of nutrition, crowding and interspecific interactions in the development of winged aphids. Ecol Entom 26(3):330–340. doi: 10.1046/j.1365-2311.2001.00321.x CrossRefGoogle Scholar
  29. 29.
    Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–230. doi: 10.1146/annurev.ento.42.1.207 CrossRefPubMedGoogle Scholar
  30. 30.
    Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97(3):192–199. doi: 10.1038/sj.hdy.6800863 CrossRefPubMedGoogle Scholar
  31. 31.
    Mueller WC, Rochow WF (1961) An aphid-injection method for the transmission of barley yellow dwarf virus. Virology 14:253–258CrossRefPubMedGoogle Scholar
  32. 32.
    Kring JB (1977) Structure of the eyes of the pea aphid, Acyrthosiphon pisum. Ann Entomol Soc Am 70(6):855–860CrossRefGoogle Scholar
  33. 33.
    Bromley AK, Dunn JA, Anderson M (1979) Ultrastructure of the antennal sensilla of aphids. I. Coeloconic and placoid sensilla. Cell Tissue Res 203(3):427–442CrossRefPubMedGoogle Scholar
  34. 34.
    Lyko F, Maleszka R (2011) Insects as innovative models for functional studies of DNA methylation. Trends Genet 27(4):127–131. doi: 10.1016/j.tig.2011.01.003 CrossRefPubMedGoogle Scholar
  35. 35.
    Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481–514. doi: 10.1146/annurev.biochem.74.010904.153721 CrossRefPubMedGoogle Scholar
  36. 36.
    Probst AV, Dunleavy E, Almouzni G (2009) Epigenetic inheritance during the cell cycle. Nat Rev Mol Cell Biol 10(3):192–206. doi: 10.1038/nrm2640 CrossRefPubMedGoogle Scholar
  37. 37.
    Suzuki MM, Bird A (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9(6):465–476. doi: 10.1038/nrg2341 CrossRefPubMedGoogle Scholar
  38. 38.
    Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13(7):484–492. doi: 10.1038/nrg3230 CrossRefPubMedGoogle Scholar
  39. 39.
    Fournier A, Sasai N, Nakao M, Defossez P-A (2012) The role of methyl-binding proteins in chromatin organization and epigenome maintenance. Brief Funct Genomics 11(3):251–264. doi: 10.1093/bfgp/elr040 CrossRefPubMedGoogle Scholar
  40. 40.
    Walsh TK, Brisson JA, Robertson HM, Gordon K, Jaubert-Possamai S, Tagu D, Edwards OR (2010) A functional DNA methylation system in the pea aphid, Acyrthosiphon pisum. Insect Mol Biol 19(Suppl 2):215–228. doi: 10.1111/j.1365-2583.2009.00974.x CrossRefPubMedGoogle Scholar
  41. 41.
    Hellman A, Chess A (2007) Gene body-specific methylation on the active X chromosome. Science 315(5815):1141–1143. doi: 10.1126/science.1136352 CrossRefPubMedGoogle Scholar
  42. 42.
    Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, Kashlev M, Oberdoerffer P, Sandberg R, Oberdoerffer S (2011) CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479(7371):74–79. doi: 10.1038/nature10442 CrossRefPubMedGoogle Scholar
  43. 43.
    Hunt BG, Glastad KM, Yi SV, Goodisman MA (2013) The function of intragenic DNA methylation: insights from insect epigenomes. Integr Comp Biol 53(2):319–328. doi: 10.1093/icb/ict003 CrossRefPubMedGoogle Scholar
  44. 44.
    Bonasio R, Li Q, Lian J, Mutti Navdeep S, Jin L, Zhao H, Zhang P, Wen P, Xiang H, Ding Y, Jin Z, Shen Steven S, Wang Z, Wang W, Wang J, Berger Shelley L, Liebig J, Zhang G, Reinberg D (2012) Genome-wide and caste-specific DNA methylomes of the ants Camponotus floridanus and Harpegnathos saltator. Curr Biol 22(19):1755–1764. doi: 10.1016/j.cub.2012.07.042 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Graf S, Huss M, Keefe D, Liu Z, London D, McDaniell RM, Shibata Y, Showers KA, Simon JM, Vales T, Wang T, Winter D, Zhang Z, Clarke ND, Birney E, Iyer VR, Crawford GE, Lieb JD, Furey TS (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 21(10):1757–1767. doi: 10.1101/gr.121541.111 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Van Holde KE (1989) Chromatin. Springer series in molecular biology. Springer, New YorkGoogle Scholar
  47. 47.
    Ho L, Crabtree GR (2010) Chromatin remodelling during development. Nature 463(7280):474–484. doi: 10.1038/nature08911 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Zhou VW, Goren A, Bernstein BE (2011) Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12(1):7–18. doi: 10.1038/nrg2905 CrossRefPubMedGoogle Scholar
  49. 49.
    Rider SD Jr, Srinivasan DG, Hilgarth RS (2010) Chromatin-remodelling proteins of the pea aphid, Acyrthosiphon pisum (Harris). Insect Mol Biol 19(Suppl 2):201–214. doi: 10.1111/j.1365-2583.2009.00972.x CrossRefPubMedGoogle Scholar
  50. 50.
    Mandrioli M, Azzoni P, Lombardo G, Manicardi GC (2011) Composition and epigenetic markers of heterochromatin in the aphid Aphis nerii (Hemiptera: Aphididae). Cytogenet Genome Res 133(1):67–77CrossRefPubMedGoogle Scholar
  51. 51.
    Mandrioli M, Borsatti F (2007) Analysis of heterochromatic epigenetic markers in the holocentric chromosomes of the aphid Acyrthosiphon pisum. Chromosome Res 15(8):1015–1022. doi: 10.1007/s10577-007-1176-4 CrossRefPubMedGoogle Scholar
  52. 52.
    Hawkins RD, Hon GC, Ren B (2010) Next-generation genomics: an integrative approach. Nat Rev Genet 11(7):476–486. doi: 10.1038/nrg2795 PubMedPubMedCentralGoogle Scholar
  53. 53.
    Fraga MF, Esteller M (2002) DNA methylation: a profile of methods and applications. BioTechniques 33(3):632, 634, 636–649Google Scholar
  54. 54.
    McKay DJ, Lieb JD (2013) A common set of DNA regulatory elements shapes Drosophila appendages. Dev Cell 27(3):306–318. doi: 10.1016/j.devcel.2013.10.009 CrossRefPubMedGoogle Scholar
  55. 55.
    The International Aphid Genomics C (2010) Genome sequence of the pea aphid (Acyrthosiphon pisum). PLoS Biol 8(2):e1000313. doi: 10.1371/journal.pbio.1000313 CrossRefGoogle Scholar
  56. 56.
    Legeai F, Shigenobu S, Gauthier JP, Colbourne J, Rispe C, Collin O, Richards S, Wilson ACC, Murphy T, Tagu D (2010) AphidBase: a centralized bioinformatic resource for annotation of the pea aphid genome. Insect Mol Biol 19:5–12. doi: 10.1111/j.1365-2583.2009.00930.x CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Zhou L, Cheng X, Connolly BA, Dickman MJ, Hurd PJ, Hornby DP (2002) Zebularine: a novel DNA methylation inhibitor that forms a covalent complex with DNA methyltransferases. J Mol Biol 321(4):591–599CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Zhou P, Lu Y, Sun XH (2011) Zebularine suppresses TGF-beta-induced lens epithelial cell-myofibroblast transdifferentiation by inhibiting MeCP2. Mol Vis 17:2717–2723PubMedPubMedCentralGoogle Scholar
  59. 59.
    Cheng JC, Matsen CB, Gonzales FA, Ye W, Greer S, Marquez VE, Jones PA, Selker EU (2003) Inhibition of DNA methylation and reactivation of silenced genes by zebularine. J Natl Cancer Inst 95(5):399–409CrossRefPubMedGoogle Scholar
  60. 60.
    Dombrovsky A, Arthaud L, Ledger TN, Tares S, Robichon A (2009) Profiling the repertoire of phenotypes influenced by environmental cues that occur during asexual reproduction. Genome Res 19(11):2052–2063. doi: 10.1101/gr.091611.109 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Mutti NS, Park Y, Reese JC, Reeck GR (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J Insect Sci 6(38):1–7. doi: 10.1673/031.006.3801 CrossRefPubMedGoogle Scholar
  62. 62.
    Jaubert-Possamai S, Le Trionnaire G, Bonhomme J, Christophides GK, Rispe C, Tagu D (2007) Gene knockdown by RNAi in the pea aphid Acyrthosiphon pisum. BMC Biotechnol 7:63. doi: 10.1186/1472-6750-7-63 CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Christiaens O, Swevers L, Smagghe G (2014) DsRNA degradation in the pea aphid (Acyrthosiphon pisum) associated with lack of response in RNAi feeding and injection assay. Peptides 53:307–314. doi: 10.1016/j.peptides.2013.12.014 CrossRefPubMedGoogle Scholar
  64. 64.
    Bhaya D, Davison M, Barrangou R (2011) CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 45:273–297. doi: 10.1146/annurev-genet-110410-132430 CrossRefPubMedGoogle Scholar
  65. 65.
    Terns MP, Terns RM (2011) CRISPR-based adaptive immune systems. Curr Opin Microbiol 14(3):321–327. doi: 10.1016/j.mib.2011.03.005 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482(7385):331–338. doi: 10.1038/nature10886 CrossRefPubMedGoogle Scholar
  67. 67.
    Pennisi E (2013) The CRISPR craze. Science 341(6148):833–836. doi: 10.1126/science.341.6148.833 CrossRefPubMedGoogle Scholar
  68. 68.
    Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821. doi: 10.1126/science.1225829 CrossRefPubMedGoogle Scholar
  69. 69.
    Terns RM, Terns MP (2014) CRISPR-based technologies: prokaryotic defense weapons repurposed. Trends Genet 30(3):111–118. doi: 10.1016/j.tig.2014.01.003 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Hsu Patrick D, Lander Eric S, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157(6):1262–1278. doi: 10.1016/j.cell.2014.05.010 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Rusk N (2014) CRISPRs and epigenome editing. Nat Methods 11(1):28CrossRefPubMedGoogle Scholar
  72. 72.
    Friedland AE, Tzur YB, Esvelt KM, Colaiacovo MP, Church GM, Calarco JA (2013) Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10(8):741–743. doi: 10.1038/nmeth.2532 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31(3):227–229. doi: 10.1038/nbt.2501 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14(1):49–55. doi: 10.1038/nrm3486 CrossRefPubMedGoogle Scholar
  75. 75.
    Maeder ML, Angstman JF, Richardson ME, Linder SJ, Cascio VM, Tsai SQ, Ho QH, Sander JD, Reyon D, Bernstein BE, Costello JF, Wilkinson MF, Joung JK (2013) Targeted DNA demethylation and activation of endogenous genes using programmable TALE-TET1 fusion proteins. Nat Biotechnol 31(12):1137–1142. doi: 10.1038/nbt.2726 CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Mendenhall EM, Williamson KE, Reyon D, Zou JY, Ram O, Joung JK, Bernstein BE (2013) Locus-specific editing of histone modifications at endogenous enhancers. Nat Biotechnol 31(12):1133–1136. doi: 10.1038/nbt.2701 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119(7):941–953. doi: 10.1016/j.cell.2004.12.012 CrossRefPubMedGoogle Scholar
  78. 78.
    Liang G, Lin JCY, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA, Jones PA (2004) Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci U S A 101(19):7357–7362. doi: 10.1073/pnas.0401866101 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Zhou P, Lu Y, Sun XH (2012) Effects of a novel DNA methyltransferase inhibitor Zebularine on human lens epithelial cells. Mol Vis 18:22–28PubMedPubMedCentralGoogle Scholar
  80. 80.
    Larson MH, Gilbert LA, Wang X, Lim WA, Weissman JS, Qi LS (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8(11):2180–2196. doi: 10.1038/nprot.2013.132 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Ghanim M, Dombrovsky A, Raccah B, Sherman A (2006) A microarray approach identifies ANT, OS-D and takeout-like genes as differentially regulated in alate and apterous morphs of the green peach aphid Myzus persicae (Sulzer). Insect Biochem Mol Biol 36(11):857–868. doi: 10.1016/j.ibmb.2006.08.007 CrossRefPubMedGoogle Scholar
  82. 82.
    Brisson JA, Davis GK, Stern DL (2007) Common genome-wide patterns of transcript accumulation underlying the wing polyphenism and polymorphism in the pea aphid (Acyrthosiphon pisum). Evol Dev 9(4):338–346. doi: 10.1111/j.1525-142X.2007.00170.x CrossRefPubMedGoogle Scholar
  83. 83.
    Purandare SR, Bickel RD, Jaquiery J, Rispe C, Brisson JA (2014) Accelerated evolution of morph-biased genes in pea aphids. Mol Biol Evol 31(8):2073–2083. doi: 10.1093/molbev/msu149 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Liu L-J, Zheng H-Y, Jiang F, Guo W, Zhou S-T (2014) Comparative transcriptional analysis of asexual and sexual morphs reveals possible mechanisms in reproductive polyphenism of the cotton aphid. PLoS One 9(6):e99506. doi: 10.1371/journal.pone.0099506 CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Cortes T, Tagu D, Simon JC, Moya A, Martinez-Torres D (2008) Sex versus parthenogenesis: a transcriptomic approach of photoperiod response in the model aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Gene 408(1–2):146–156. doi: 10.1016/j.gene.2007.10.030 CrossRefPubMedGoogle Scholar
  86. 86.
    Le Trionnaire G, Francis F, Jaubert-Possamai S, Bonhomme J, De Pauw E, Gauthier JP, Haubruge E, Legeai F, Prunier-Leterme N, Simon JC, Tanguy S, Tagu D (2009) Transcriptomic and proteomic analyses of seasonal photoperiodism in the pea aphid. BMC Genomics 10:456. doi: 10.1186/1471-2164-10-456 CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Steel CG, Lees AD (1977) The role of neurosecretion in the photoperiodic control of polymorphism in the aphid Megoura viciae. J Exp Biol 67:117–135PubMedGoogle Scholar
  88. 88.
    Le Trionnaire G, Jaubert-Possamai S, Bonhomme J, Gauthier JP, Guernec G, Le Cam A, Legeai F, Monfort J, Tagu D (2012) Transcriptomic profiling of the reproductive mode switch in the pea aphid in response to natural autumnal photoperiod. J Insect Physiol 58(12):1517–1524. doi: 10.1016/j.jinsphys.2012.07.009 CrossRefPubMedGoogle Scholar
  89. 89.
    Le Trionnaire G, Jaubert S, Sabater-Munoz B, Benedetto A, Bonhomme J, Prunier-Leterme N, Martinez-Torres D, Simon JC, Tagu D (2007) Seasonal photoperiodism regulates the expression of cuticular and signalling protein genes in the pea aphid. Insect Biochem Mol Biol 37(10):1094–1102. doi: 10.1016/j.ibmb.2007.06.008 CrossRefPubMedGoogle Scholar
  90. 90.
    Gallot A, Shigenobu S, Hashiyama T, Jaubert-Possamai S, Tagu D (2012) Sexual and asexual oogenesis require the expression of unique and shared sets of genes in the insect Acyrthosiphon pisum. BMC Genomics 13:76. doi: 10.1186/1471-2164-13-76 CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Le Trionnaire G, Wucher V, Tagu D (2013) Genome expression control during the photoperiodic response of aphids. Physiol Entomol 38(2):117–125. doi: 10.1111/phen.12021 CrossRefGoogle Scholar
  92. 92.
    Gallot A, Rispe C, Leterme N, Gauthier J-P, Jaubert-Possamai S, Tagu D (2010) Cuticular proteins and seasonal photoperiodism in aphids. Insect Biochem Mol Biol 40(3):235–240. doi: 10.1016/j.ibmb.2009.12.001 CrossRefPubMedGoogle Scholar
  93. 93.
    Ma Z, Guo W, Guo X, Wang X, Kang L (2011) Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proc Natl Acad Sci 108(10):3882–3887. doi: 10.1073/pnas.1015098108 CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Hardie JIM, Lees AD (1985) The induction of normal and teratoid viviparae by a juvenile hormone and kinoprene in two species of aphids. Physiol Entomol 10(1):65–74. doi: 10.1111/j.1365-3032.1985.tb00020.x CrossRefGoogle Scholar
  95. 95.
    Hardie J, Gao N, Timar T, Sebok P, Honda K (1996) Precocene derivatives and aphid morphogenesis. Arch Insect Biochem Physiol 32(3–4):493–501. doi: 10.1002/(sici)1520-6327(1996)32:3/4<493::aid-arch21>3.0.co;2-6 CrossRefGoogle Scholar
  96. 96.
    Ishikawa A, Ishikawa Y, Okada Y, Miyazaki S, Miyakawa H, Koshikawa S, Brisson JA, Miura T (2012) Screening of upregulated genes induced by high density in the vetch aphid Megoura crassicauda. J Exp Zool A Ecol Genet Physiol 317(3):194–203. doi: 10.1002/jez.1713 CrossRefPubMedGoogle Scholar
  97. 97.
    Schwedes CC, Carney GE (2012) Ecdysone signaling in adult Drosophila melanogaster. J Insect Physiol 58(3):293–302. doi: 10.1016/j.jinsphys.2012.01.013 CrossRefPubMedGoogle Scholar
  98. 98.
    Miura T, Braendle C, Shingleton A, Sisk G, Kambhampati S, Stern DL (2003) A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J Exp Zool B Mol Dev Evol 295(1):59–81. doi: 10.1002/jez.b.3 CrossRefPubMedGoogle Scholar
  99. 99.
    Ishikawa A, Miura T (2013) Transduction of high-density signals across generations in aphid wing polyphenism. Physiol Entomol 38(2):150–156. doi: 10.1111/phen.12022 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Mary Grantham
    • 1
  • Jennifer A. Brisson
    • 1
  • Denis Tagu
    • 2
  • Gael Le Trionnaire
    • 2
    Email author
  1. 1.Department of BiologyUniversity of RochesterRochesterUSA
  2. 2.UMR 1349 (INRA – Agrocampuus Ouest – University of Rennes I) IGEPP – Institute of Genetics Environment and Plant ProtectionRennes, Le Rheu cedexFrance

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