Skip to main content
Log in

Transcriptome Profiling of Neurosensory Perception Genes in Wing Tissue of Two Evolutionary Distant Insect Orders: Diptera (Drosophila melanogaster) and Hemiptera (Acyrthosiphon pisum)

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The neurogenesis and neuronal functions in insect wing have been understudied mainly due to technical hindrances that have prevented electrophysiology studies for decades. The reason is that the nano-architecture of the wing chemosensory bristles hampers the receptors accessibility of odorants/tastants to receptors in fixed setup, whereas in nature, the wing flapping mixes these molecules in bristle lymph. In this report, we analyzed the transcriptome of the wing tissue of two species phylogenetically strongly divergent: Drosophila melanogaster a generic model for diptera order (complete metamorphosis) and the aphid acyrthosiphon pisum, representative of hemiptera order (incomplete metamorphosis) for which a conditional winged/wingless polyphenism is under control of population density and resources. The transcriptome shows that extensive gene networks involved in chemosensory perception are active in adult wing for both species. Surprisingly, the specific transcripts of genes that are commonly found in eye were present in Drosophila wing but not in aphid. The analysis reveals that in the aphid conditional wing, expressed genes show strong similarities with those in the gut epithelia. This suggests that the epithelial cell layer between the cuticle sheets is persistent at least in young aphid adult, whereas it disappears after emergence in Drosophila. Despite marked differences between the two transcriptomes, the results highlight the probable universalism of wing chemosensory function in the holometabolous and hemimetabolous orders of winged insects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ashkenas J, Muschler J, Mina J, Bissell MJ (1996). The extracellular matrix in epithelial biology: shared molecules and common themes in distant phyla. Dev Biol 180:433–444

    Article  CAS  PubMed  Google Scholar 

  • Belalcazar AD, Doyle K, Hogan J, Neff D, Collier S (2013) Insect wing membrane topography is determined by the dorsal wing epithelium. G3 (Bethesda) 3:5–8

    Article  Google Scholar 

  • Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97:192–199

    Article  CAS  PubMed  Google Scholar 

  • Brisson JA, Stern DC (2006) The pea aphid Acyrthosiphon pisum: an emerging genome model system for ecological developmental evolutionary studies. Biossays, 28:747–755

    Article  CAS  Google Scholar 

  • Brisson JA, Davis GK, Stern DL (2007) Common genome-wide patterns of transcript accumulation underlying the wing polyphenism and polymorphism in the pea aphid. Evol Dev 9:338–346

    Article  CAS  PubMed  Google Scholar 

  • Cameron P, Hiroi M, Ngai J, Scott K 2010. The molecular basis for water taste in Drosophila. Nature, 465:91–95

  • Cho EH, Nijhout HF (2013) Development of polyploidy of scale-building cells in the wings of Manduca sexta. Arthropod Struct Dev 42:37–46

    Article  PubMed  Google Scholar 

  • Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830–1834

    Article  CAS  PubMed  Google Scholar 

  • Dickinson M (2006) Insect flight. Curr Biol 16:R309-14

    Article  PubMed  Google Scholar 

  • Dickinson MH, Lehmann FO, Sane SP (1999) Wing rotation and the aerodynamic basis of insect flight. Science 284:1954–1960

    Article  CAS  PubMed  Google Scholar 

  • Dixon A.F.G. (1998) Aphid Ecology. Chapman & Hall, London

    Google Scholar 

  • Hartenstein V, Posakony JW (1989) Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development 107:389–405

    CAS  PubMed  Google Scholar 

  • Hkmat-Scafe DS, Scafe CR, Mckinney AJ, Tanouye MA (2002) Genome-wide analysis of the odorant-binding protein gene family in Drosophila melanogaster. Genome Res 12:1357–1369

    Article  Google Scholar 

  • Johnson SA, Milner MJ (1987) The final stages of wing development in Drosophila melanogaster. Tissue Cell 19:505–513

    Article  CAS  PubMed  Google Scholar 

  • Kiger JA, Natzle JE, Kimbrell DA, Paddy MR, Kleinhesselink K, Green MM (2007) Tissue remodeling during maturation of the Drosophila wing. Dev Biol 301:178–191

    Article  CAS  PubMed  Google Scholar 

  • Kimura KI, Kodama A, Hayasaka Y, Takumi Ohta T (2004) Activation of the cAMP/PKA signaling pathway is required for postecdysial cell death in wing epidermal cells of Drosophila melanogaster. Development 131:1597–1606

    Article  CAS  PubMed  Google Scholar 

  • Labandeira C, Phillips T (1996) A carboniferous insect gall: insight into the early ecological history of the Holometabola. Proc Natl Acad Sci USA 93:8470–8474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Misof B et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767

    Article  CAS  PubMed  Google Scholar 

  • Ogawa K, Miura T (2013) Two developmental switch points for the wing polymorphisms in the pea aphid Acyrthosiphon pisum. Evol Dev 4:30

    Google Scholar 

  • Peters RS et al (2014) The evolutionary history of holometabolous insects inferred from transcriptome-based phylogeny and comprehensive morphological data. BMC Evol Biol 14:52

    Article  PubMed  PubMed Central  Google Scholar 

  • Raad H, Ferveur JF, Ledger N, Capovilla M, Robichon A (2016) Functional gustatory role of chemoreceptors in Drosophila Wings. Cell Rep 15:1442–1454

    Article  CAS  PubMed  Google Scholar 

  • Reynolds SE (1977) Control of cuticle extensibility in the wings of adult Manduca at the time of eclosion: effects of eclosion hormone and bursicon. J Exp Biol 70:27–30

    CAS  Google Scholar 

  • Scott K et al (2001) Chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661–673

    Article  CAS  PubMed  Google Scholar 

  • Seligman IM, Doy FA, Crossley AC (1975) Hormonal control of morphogenetic cell death of the wing hypodermis in Lucilia cuprina. Tissue Cell 7:281–296

    Article  CAS  PubMed  Google Scholar 

  • Smadja C. Shi P, Butlin RK, Hugh M, Robertson HM (2009) Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum. Mol Biol Evol 26:2073–2086

    Article  CAS  PubMed  Google Scholar 

  • Starostina E, Xu A, Lin H, Pikielny CW (2009) A Drosophila protein family implicated in pheromone perception is related to Tay-Sachs GM2-activator protein. J Biol Chem 284:585–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stocker RF (1994) The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3–26

    Article  CAS  PubMed  Google Scholar 

  • Valmalette JC, Raad H, Qiu N, Ohara S, Capovilla M, Robichon A (2015) Nano architecture of gustatory chemosensory bristles and trachea in Drosophila wings. Sci Rep 5:14198

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira FG, Rozas J (2011) Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 3:476–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are very grateful to Jean François Ferveur for fruitful discussions. The Drosophila Bloomington Stock Center is acknowledged for fly stocks. We thank a lot Aviv Dombrovsky and Jean Christophe Valmalette that gave rise to this manuscript, inspired by an initial work brought together. This work was supported by the ANR “blanc,” acronym: “Gustaile,” and the ANR “blanc,” acronym “methylclonome,” and by the French Government (National Research Agency, ANR) through the LABEX SIGNALIFE program (reference # ANR-11-LABX-0028-01).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alain Robichon.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agnel, S., da Rocha, M. & Robichon, A. Transcriptome Profiling of Neurosensory Perception Genes in Wing Tissue of Two Evolutionary Distant Insect Orders: Diptera (Drosophila melanogaster) and Hemiptera (Acyrthosiphon pisum). J Mol Evol 85, 234–245 (2017). https://doi.org/10.1007/s00239-017-9814-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-017-9814-8

Keywords

Navigation