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PLOS ONE  2012 

Differential Involvement of Hedgehog Signaling in Butterfly Wing and Eyespot Development

DOI: 10.1371/journal.pone.0051087

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Abstract:

Butterfly eyespots may have evolved from the recruitment of pre-existent gene circuits or regulatory networks into novel locations on the wing. Gene expression data suggests one such circuit, the Hedgehog (Hh) signaling pathway and its target gene engrailed (en), was recruited from a role in patterning the anterior-posterior insect wing axis to a role patterning butterfly eyespots. However, while Junonia coenia expresses hh and en both in the posterior compartment of the wing and in eyespot centers, Bicyclus anynana lacks hh eyespot-specific expression. This suggests that Hh signaling may not be functioning in eyespot development in either species or that it functions in J. coenia but not in B. anynana. In order to test these hypotheses, we performed functional tests of Hh signaling in these species. We investigated the effects of Hh protein sequestration during the larval stage on en expression levels, and on wing size and eyespot size in adults. Hh sequestration led to significantly reduced en expression and to significantly smaller wings and eyespots in both species. But while eyespot size in B. anynana was reduced proportionately to wing size, in J. coenia, eyespots were reduced disproportionately, indicating an independent role of Hh signaling in eyespot development in J. coenia. We conclude that while Hh signaling retains a conserved role in promoting wing growth across nymphalid butterflies, it plays an additional role in eyespot development in some, but not all, lineages of nymphalid butterflies. We discuss our findings in the context of alternative evolutionary scenarios that led to the differential expression of hh and other Hh pathway signaling members across nymphalid species.

References

[1]  True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evolution & Development 3: 109–119.
[2]  Wang XY, Sommer RJ (2011) Antagonism of LIN-17/Frizzled and LIN-18/Ryk in Nematode Vulva Induction Reveals Evolutionary Alterations in Core Developmental Pathways. PLoS Biology 9: e1001110.
[3]  Lynch JA, Brent AE, Leaf DS, Pultz MA, Desplan C (2006) Localized maternal orthodenticle patterns anterior and posterior in the long germ wasp Nasonia. Nature 439: 728–732.
[4]  Schroder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422: 621–625.
[5]  McGregor AP (2006) Wasps, beetles and the beginning of the ends. BioEssays 28: 683–686.
[6]  Oliver JC, Tong X, Gall LF, Piel WH, Monteiro A (2012) A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression. PLoS Genet 8(8): e1002893.
[7]  Shirai LT, Saenko SV, Keller RA, Jeronimo MA, Brakefield PM, et al. (2012) Evolutionary history of the recruitment of conserved developmental genes in association to the formation and diversification of a novel trait. BMC Evol Biol 12: 21.
[8]  Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, et al. (1999) Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532–534.
[9]  Saenko SV, Marialva MSP, Beldade P (2011) Involvement of the conserved Hox gene Antennapedia in the development and evolution of a novel trait. EvoDevo 2: 9.
[10]  Terenius O, Papanicolaou A, Garbutt JS, Eleftherianos I, Huvenne H, et al. (2011) RNA interference in Lepidoptera: An overview of successful and unsuccessful studies and implications for experimental design. J Insect Physiol 57: 231–245.
[11]  Aste-Amezaga M, Zhang NY, Lineberger JE, Arnold BA, Toner TJ, et al. (2010) Characterization of Notch1 Antibodies That Inhibit Signaling of Both Normal and Mutated Notch1 Receptors. PLoS ONE 5: e9094.
[12]  Fukasawa H, Yamamoto T, Suzuki H, Togawa A, Ohashi N, et al. (2004) Treatment with anti-TGF-beta antibody ameliorates chronic progressive nephritis by inhibiting Smad/TGF-beta signaling. Kidney International 65: 63–74.
[13]  Stockwin LH, Holmes S (2003) Antibodies as therapeutic agents: vive la renaissance! Expert Opinion on Biological Therapy. 3: 1133–1152.
[14]  Incardona JP, Lee JH, Robertson CP, Enga K, Kapur RP, et al. (2000) Receptor-mediated endocytosis of soluble and membrane-tethered Sonic hedgehog by Patched-1. Proc Nat Acad Sci USA 97: 12044–12049.
[15]  Ericson J, Morton S, Kawakami A, Roelink H, Jessell TM (1996) Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661–673.
[16]  De Rivoyre M, Ruel L, Varjosalo M, Loubat A, Bidet M, et al. (2006) Human receptors patched and smoothened partially transduce hedgehog signal when expressed in Drosophila cells. J Biol Chem 281: 28584–28595.
[17]  Porter JA, von Kessler DP, Ekker SC, Young KE, Lee JJ, et al. (1995) The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374: 363–366.
[18]  Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797.
[19]  Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876–4882.
[20]  Nicholas KB, Jr NHB, Deerfield DWI (1997) GeneDoc: Analysis and Visualization of Genetic Variation. EMBNETnews. 1–4.
[21]  Lee JJ, Ekker SC, von Kessler DP, Porter JA, Sun BI, et al. (1994) Autoproteolysis in hedgehog Protein Biogenesis. Science 266: 1528–1537.
[22]  Zhao Y, Tong C, Jiang J (2007) Hedgehog regulates smoothened activity by inducing a conformational switch. Nature 450: 252–258.
[23]  Monteiro A, Pierce NE (2001) Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII and EF-1a gene sequences. Mol Phylogen Evol 18: 264–281.
[24]  Vischer NOE, Huls PG, Woldringh CL (1994) Object-Image: An interactive image analysis program using structured point collection. Binary (Bioline) 6.
[25]  Strigini M, Cohen SM (1997) A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124: 4697–4705.
[26]  Bosanac I, Maun HR, Scales SJ, Wen XH, Lingel A, et al. (2009) The structure of SHH in complex with HHIP reveals a recognition role for the Shh pseudo active site in signaling. Nature Struct Mol Biol 16: 691–697.
[27]  Maun HR, Wen XH, Lingel A, de Sauvage FJ, Lazarus RA, et al. (2010) Hedgehog Pathway Antagonist 5E1 Binds Hedgehog at the Pseudo-active Site. J Biol Chem 285: 26570–26580.
[28]  Bossing T, Brand AH (2006) Determination of cell fate along the anteroposterior axis of the Drosophila ventral midline. Development 133: 1001–1012.
[29]  Duman-Scheel M, Weng L, Xin S, Du W (2002) Hedgehog regulates cell growth and proliferation by inducing Cyclin D and Cyclin E. Nature. 417: 299–304.
[30]  Rowitch DH, S-Jacques B, Lee SM, Flax JD, Snyder EY, et al. (1999) Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J Neurosci 19: 8954–8965.
[31]  Hervold K, Martin A, Kirkpatrick RA, Mc Kenna PF, Ramirez-Weber FA (2007) Hedgehog Signaling Pathway Database: a repository of current annotation efforts and resources for the Hh research community. Nucleic Acids Res 35: D595–D598.
[32]  Ruiz i Altaba A (1999) Gli proteins and Hedgehog signaling: development and cancer. Trends Genet 15: 418–425.
[33]  Pasca di Magliano M, Hebrok M (2003) Hedgehog signalling in cancer formation and maintenance. Nat Rev Cancer 3: 903–911.
[34]  Basler K, Struhl G (1994) Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368: 208–214.
[35]  Bejarano F, Perez L, Apidianakis Y, Delidakis C, Milan M (2007) Hedgehog restricts its expression domain in the Drosophila wing. EMBO Rep 8: 778–783.
[36]  Johnson RL, Grenier JK, Scott MP (1995) patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development 121: 4161–4170.
[37]  Burglin TR (2008) The Hedgehog protein family. Genome Biol 9: 241.
[38]  Matson CK, Zarkower D (2012) Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Genet 13: 163–174.

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