Letter | Published:

Two insulin receptors determine alternative wing morphs in planthoppers

Nature volume 519, pages 464467 (26 March 2015) | Download Citation

Abstract

Wing polyphenism is an evolutionarily successful feature found in a wide range of insects1. Long-winged morphs can fly, which allows them to escape adverse habitats and track changing resources, whereas short-winged morphs are flightless, but usually possess higher fecundity than the winged morphs1,2,3. Studies on aphids, crickets and planthoppers have revealed that alternative wing morphs develop in response to various environmental cues1,2,4,5,6,7,8, and that the response to these cues may be mediated by developmental hormones, although research in this area has yielded equivocal and conflicting results about exactly which hormones are involved4,8,9,10. As it stands, the molecular mechanism underlying wing morph determination in insects has remained elusive. Here we show that two insulin receptors in the migratory brown planthopper Nilaparvata lugens, InR1 and InR2, have opposing roles in controlling long wing versus short wing development by regulating the activity of the forkhead transcription factor Foxo. InR1, acting via the phosphatidylinositol-3-OH kinase (PI(3)K)–protein kinase B (Akt) signalling cascade, leads to the long-winged morph if active and the short-winged morph if inactive. InR2, by contrast, functions as a negative regulator of the InR1–PI(3)K–Akt pathway: suppression of InR2 results in development of the long-winged morph. The brain-secreted ligand Ilp3 triggers development of long-winged morphs. Our findings provide the first evidence of a molecular basis for the regulation of wing polyphenism in insects, and they are also the first demonstration—to our knowledge—of binary control over alternative developmental outcomes, and thus deepen our understanding of the development and evolution of phenotypic plasticity.

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Accessions

Data deposits

The cDNA sequences of NlInR1 and NlInR2 have been deposited in GenBank under accession numbers KF974333 and KF974334, respectively. Gene sequences used for dsRNA synthesis have been deposited in GenBank under the following accession numbers: KF974335 (NlChico), KF974336 (NlLnk), KF974337 (NlAkt), KF974338 (NlPten), KF974339 (NlFoxo), KF974340KF974343 (NlIlp1–4), KF974348 (NlErk), KF974349 (NlRaf), KF974350 (NlTor), KM099280 (NlRaptor), KM099281 (NlRheb), KF974344 (SfInR1), KF974345 (SfInR2), KF974346 (LsInR1) and KF974347 (LsInR2).

References

  1. 1.

    in Phenotypic Plasticity of Insects: Mechanisms and Consequences (eds & ) 609–653 (Science, 2009)

  2. 2.

    & Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42, 207–230 (1997)

  3. 3.

    & Differential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket. Proc. Natl Acad. Sci. USA 99, 16829–16834 (2002)

  4. 4.

    , & Crowding and host plant nutrition: environmental determinants of wing-form in Prokelisia marginata. Ecology 66, 1588–1596 (1985)

  5. 5.

    Control mechanisms of polyphenic development in insects. Bioscience 49, 181–192 (1999)

  6. 6.

    , , & Genetic variation for an aphid wing polyphenism is genetically linked to a naturally occurring wing polymorphism. Proc. R. Soc. Lond. B 272, 657–664 (2005)

  7. 7.

    & The evolution and genetics of migration in insects. Bioscience 57, 155–164 (2007)

  8. 8.

    , & Polyphenism in insects. Curr. Biol. 21, R738–R749 (2011)

  9. 9.

    Action of juvenile hormone mimics on the regulation of larval–adult and alary polymorphism in aphids. Nature 267, 46–48 (1977)

  10. 10.

    , , & Wing dimorphism in aphids. Heredity 97, 192–199 (2006)

  11. 11.

    Effect of crowding during the larval period on the determination of the wing-form of an adult plant-hopper. Nature 178, 641–642 (1956)

  12. 12.

    , & Immigration of the brown planthopper, Nilaparvata lugens, exhibiting various responses to density in relation to wing morphism. Entomol. Exp. Appl. 38, 101–108 (1985)

  13. 13.

    & Effects of juvenile hormone and rearing density on wing dimorphism and oöcyte development in the brown planthopper, Nilaparvata lugens. J. Insect Physiol. 32, 585–590 (1986)

  14. 14.

    , , , & Fluctuations and factors affecting the wing-form ratio of the brown panthopper, Nilaparvata lugens Stal in rice fields. Jap. J. Appl. Entomol. Zool. 46, 135–143 (2002)

  15. 15.

    & in Insect Endocrinology (ed. ) 464–522 (Elsevier, 2012)

  16. 16.

    et al. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr. Biol. 11, 213–221 (2001)

  17. 17.

    et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104 (2001)

  18. 18.

    , & Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22, 818–835 (2001)

  19. 19.

    & Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13, 79–85 (2003)

  20. 20.

    How flies get their size: genetics meets physiology. Nature Rev. Genet. 7, 907–916 (2006)

  21. 21.

    , & Critical nodes in signalling pathways: insights into insulin action. Nature Rev. Mol. Cell Biol. 7, 85–96 (2006)

  22. 22.

    & Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43, 389–410 (2009)

  23. 23.

    Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem. J. 425, 13–26 (2010)

  24. 24.

    , & Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J. 31, 1916–1930 (2012)

  25. 25.

    , , , & Drosophila’s insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2, 239–249 (2002)

  26. 26.

    The phosphoinositide 3-kinase pathway. Science 296, 1655–1657 (2002)

  27. 27.

    et al. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994–999 (1997)

  28. 28.

    , , & Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17, 2006–2020 (2003)

  29. 29.

    & PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol. 9, 125–128 (1999)

  30. 30.

    , & TOR signaling in growth and metabolism. Cell 124, 471–484 (2006)

  31. 31.

    et al. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol. 15, 521 (2014)

  32. 32.

    et al. Genome-wide screening for components of small interfering RNA (siRNA) and micro-RNA (miRNA) pathways in the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Insect Mol. Biol. 22, 635–647 (2013)

  33. 33.

    A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45 (2001)

  34. 34.

    & A simplified procedure for a rapid and reliable assay of both glycogen and trehalose in whole yeast cells. Anal. Biochem. 248, 186–188 (1997)

  35. 35.

    et al. Molecular characterization of the flightin gene in the wing-dimorphic planthopper, Nilaparvata lugens, and its evolution in Pancrustacea. Insect Biochem. Mol. Biol. 43, 433–443 (2013)

  36. 36.

    & in Invertebrate Tissue Culture (ed. ) 307–337 (Academic, 1971)

  37. 37.

    , & Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 10, 199–207 (2009)

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Acknowledgements

We thank R.-Z. Zhang for help with BPH imaging (Fig. 1a). This work was supported by the National Basic Research Program of China (973 Program, no. 2010CB126205) and by the National Science Foundation of China (no. 31201509 and no. 31471765).

Author information

Author notes

    • Hai-Jun Xu
    •  & Jian Xue

    These authors contributed equally to this work.

Affiliations

  1. State Key Laboratory of Rice Biology and Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Sciences, Zhejiang University, Hangzhou 310058, China

    • Hai-Jun Xu
    • , Jian Xue
    • , Bo Lu
    • , Xue-Chao Zhang
    • , Ji-Chong Zhuo
    • , Shu-Fang He
    • , Xiao-Fang Ma
    • , Ya-Qin Jiang
    • , Hai-Wei Fan
    • , Ji-Yu Xu
    • , Yu-Xuan Ye
    • , Peng-Lu Pan
    • , Qiao Li
    • , Yan-Yuan Bao
    •  & Chuan-Xi Zhang
  2. Department of Biology, Duke University, Durham, North Carolina 27708, USA

    • H. Frederik Nijhout

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Contributions

H.-J.X. conceived and designed the study, wrote the paper, helped perform experiments and analysed the data. J.X. performed most experiments and helped with data analysis. B.L., Y.-Q.J., Q.L., S.-F.H. and J.-Y.X. helped perform experiments and antibody preparation. X.-C.Z. and J.-C.Z. performed gene cloning and immunoprecipitation. X.-F.M. performed RACE experiments. H.-W.F., Y.-X.Y. and P.-L.P. performed qRT–PCR. Y.-Y.B. and H.F.N. discussed data and revised the manuscript. C.-X.Z. organized and directed the project.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Hai-Jun Xu or Chuan-Xi Zhang.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary information

    This file contains Supplementary notes 1-9 and Supplementary References.

Excel files

  1. 1.

    Supplementary Data

    This file contains Supplementary Table 1 which shows the sex ratio of BPHs following dsNlInRs treatments.

  2. 2.

    Supplementary Data

    This file contains Supplementary Table 2, a list of the main primers used in this study.

Videos

  1. 1.

    An immunofluorescence assay of NlILP3 in brains of 5th-instar nymphs

    The stained nerve cords (red) were crossed over a short distance from the medial neurosecretory cells to extend backwards in an arc through the brain. The cell nucleus is stained with DAPI (blue).

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DOI

https://doi.org/10.1038/nature14286

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