Two insulin receptors determine alternative wing morphs in planthoppers

Nature

Volumn 519, Issue 7544, 2015, Pages 464-467

  Xu, Hai Jun ^a   Xue, Jian ^a   Lu, Bo ^a   Zhang, Xue Chao ^a   Zhuo, Ji Chong ^a   He, Shu Fang ^a   Ma, Xiao Fang ^a   Jiang, Ya Qin ^a   Fan, Hai Wei ^a   Xu, Ji Yu ^a   Ye, Yu Xuan ^a   Pan, Peng Lu ^a   Li, Qiao ^a   Bao, Yan Yuan ^a   Nijhout, H Frederik ^b   Zhang, Chuan Xi ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRANSCRIPTION FACTOR FOXO; FORKHEAD TRANSCRIPTION FACTOR; INSULIN;

BRAIN; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL CUE; ENZYME ACTIVITY; FLY; HABITAT TYPE; HORMONE; LIGAND; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; PLANTHOPPER; WING MORPHOLOGY;

ANIMAL EXPERIMENT; ARTICLE; FEMALE; FORELIMB; MALE; NILAPARVATA LUGENS; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPIC PLASTICITY; POLYPHENISM; PRIORITY JOURNAL; ANATOMY AND HISTOLOGY; ANIMAL; DEFICIENCY; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEMIPTERA; METABOLISM; MOLECULAR GENETICS; SIGNAL TRANSDUCTION;

APHIDIDAE; ARCHAEORRHYNCHA; GRYLLIDAE; HEXAPODA; NILAPARVATA LUGENS;

ANIMALS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HEMIPTERA; INSULIN; MALE; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION; WING;

EID: 84925780243     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14286     Document Type: Article

References (37)

1. Zera, A. J. in Phenotypic Plasticity of Insects: Mechanisms and Consequences (eds Whitman, D. W. & Ananthakrishnan, T. N.) 609-653 (Science, 2009).
2. Zera, A. J. & Denno, R. F. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42, 207-230 (1997).
3. Zhao, Z. & Zera, A. J. 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. Denno, R. F., Douglas, L. W. & Jacobs, D. Crowding and host plant nutrition: environmental determinants of wing-form in Prokelisia marginata. Ecology 66, 1588-1596 (1985).
5. Nijhout, H. F. Control mechanisms of polyphenic development in insects. Bioscience 49, 181-192 (1999).
6. Braendle, C., Friebe, I., Caillaud, M. C. & Stern, D. L. 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. Roff, D. A. & Fairbairn, D. J. The evolution and genetics of migration in insects. Bioscience 57, 155-164 (2007).
8. Simpson, S. J., Sword, G. A. & Lo, N. Polyphenism in insects. Curr. Biol. 21, R738-R749 (2011).
9. Lees, A. D. Action of juvenile hormone mimics on the regulation of larval-adult and alary polymorphism in aphids. Nature 267, 46-48 (1977).
10. Braendle, C., Davis, G. K., Brisson, J. A. & Stern, D. L. Wing dimorphism in aphids. Heredity 97, 192-199 (2006).
11. Kisimoto, R. 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. Iwanaga, K., Tojo, S. & Nagata, T. 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. Iwanaga, K. & Tojo, S. 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. Syobu, S., Mikuriya, H., Yamaguchi, J., Matsuzaki, M. & Matsumura, M. 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. Hartfelder, K. & Emlen, D. in Insect Endocrinology (ed. Gilbert, L. I.) 464-522 (Elsevier, 2012).
16. Brogiolo, W. 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. Clancy, D. J. et al. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292, 104 (2001).
18. Nakae, J., Kido, Y. & Accili, D. Distinct and overlapping functions of insulin and IGF-I receptors. Endocr. Rev. 22, 818-835 (2001).
19. Oldham, S. & Hafen, E. Insulin/IGF and target of rapamycin signaling: a TOR de force in growth control. Trends Cell Biol. 13, 79-85 (2003).
20. Edgar, B. A. How flies get their size: genetics meets physiology. Nature Rev. Genet. 7, 907-916 (2006).
21. Taniguchi, C. M., Emanuelli, B. & Kahn, C. R. Critical nodes in signalling pathways: insights into insulin action. Nature Rev. Mol. Cell Biol. 7, 85-96 (2006).
22. Hietakangas, V. & Cohen, S. M. Regulation of tissue growth through nutrient sensing. Annu. Rev. Genet. 43, 389-410 (2009).
23. Teleman, A. A. Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem. J. 425, 13-26 (2010).
24. Marshall, L., Rideout, E. J. & Grewal, S. S. Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J. 31, 1916-1930 (2012).
25. Britton, J. S., Lockwood, W. K., Li, L., Cohen, S. M. & Edgar, B. A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2, 239-249 (2002).
26. Cantley, L. C. The phosphoinositide 3-kinase pathway. Science 296, 1655-1657 (2002).
27. Ogg, S. 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. Puig, O., Marr, M. T., Ruhf, M. L. & Tjian, R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17, 2006-2020 (2003).
29. Maehama, T. & Dixon, J. E. PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol. 9, 125-128 (1999).
30. Wullschleger, S., Loewith, R.& Hall, M. N. TOR signaling in growth andmetabolism. Cell 124, 471-484 (2006).
31. Xue, J. 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. Xu, H. J. 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. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).
34. Parrou, J. L. & Francois, J. 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. Xue, J. 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. Hirumi, H. & Maramorosch, K. in Invertebrate Tissue Culture (ed. Vago, C.) 307-337 (Academic, 1971).
37. Géminard, C., Rulifson, E. J. & Leópold, P. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab. 10, 199-207 (2009).