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Ancient Expansion of the Hox Cluster in Lepidoptera Generated Four Homeobox Genes Implicated in Extra-Embryonic Tissue Formation


We have examined gene duplication in a set of ancient genes used in patterning of animal embryos:
the Hox genes. These genes code for proteins that bind DNA and switch on or off other genes, and they are very similar between distantly related animal species. Butterflies and moths, however, have additional Hox genes whose origin and role has been unclear. We have sequenced the genomes of five species of butterfly and moth, and of a closely related caddisfly, to examine these issues. We found that one of the Hox genes, called zen, duplicated to generate four new genes in the evolution of the largest group of butterflies and moths. Further mutations greatly modified the DNA sequence of the new genes, although maintaining potential to encode stable protein folds. Gene expression also changed so that the new Hox-derived genes are deployed in egg and early embryonic stages marking the tissues that will later envelop, nourish and protect the embryo.


Vyšlo v časopise: Ancient Expansion of the Hox Cluster in Lepidoptera Generated Four Homeobox Genes Implicated in Extra-Embryonic Tissue Formation. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004698
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004698

Souhrn

We have examined gene duplication in a set of ancient genes used in patterning of animal embryos:
the Hox genes. These genes code for proteins that bind DNA and switch on or off other genes, and they are very similar between distantly related animal species. Butterflies and moths, however, have additional Hox genes whose origin and role has been unclear. We have sequenced the genomes of five species of butterfly and moth, and of a closely related caddisfly, to examine these issues. We found that one of the Hox genes, called zen, duplicated to generate four new genes in the evolution of the largest group of butterflies and moths. Further mutations greatly modified the DNA sequence of the new genes, although maintaining potential to encode stable protein folds. Gene expression also changed so that the new Hox-derived genes are deployed in egg and early embryonic stages marking the tissues that will later envelop, nourish and protect the embryo.


Zdroje

1. McGinnisW, KrumlaufR (1992) Homeobox genes and axial patterning. Cell 68: 283–302.

2. KappenC, SchughartK, RuddleFH (1989) Two steps in the evolution of Antennapedia-class vertebrate homeobox genes. Proc Natl Acad Sci USA 86: 5459–5463.

3. de RosaR, GrenierJK, AndreevaT, CookCE, AdoutteA, et al. (1999) Hox genes in brachiopods and priapulids and protostome evolution. Nature 399: 772–776.

4. DubouleD (2007) The rise and fall of Hox gene clusters. Development 134: 2549–2560.

5. LemonsD, McGinnisW (2006) Genomic evolution of Hox gene clusters. Science 313: 1918–1922.

6. SimakovO, MarlétazF, ChoSJ, Edsinger-GonzalesE, HavlakP, et al. (2013) Insights into bilaterian evolution from three spiralian genomes. Nature 493: 526–531.

7. ZhangG, FangX, GuoX, LiL, LuoR, et al. (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490: 49–54.

8. PowersTP, AmemiyaCT (2004) Evidence for a Hox14 paralog group in vertebrates. Curr Biol 14: R183–184.

9. HollandLZ, AlbalatR, AzumiK, Benito-GutierrezE, BlowMJ, et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18: 1100–1111.

10. SchughartK, KappenC, RuddleFH (1989) Duplication of large genomic regions during the evolution of vertebrate homeobox genes. Proc Natl Acad Sci USA 86: 7067–7071.

11. BrownSJ, FellersJP, ShippyTD, RichardsonEA, MaxwellM, et al. (2002) Sequence of the Tribolium castaneum homeotic complex: the region corresponding to the Drosophila melanogaster antennapedia complex. Genetics 160: 1067–1074.

12. StauberM, JackleH, Schmidt-OttU (1999) The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc Natl Acad Sci U S A 96: 3786–3789.

13. NegreB, CasillasS, SuzanneM, Sánchez-HerreroE, AkamM, et al. (2005) Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex. Genome Res 15: 692–700.

14. FalcianiF, HausdorfB, SchröderR, AkamM, TautzD, et al. (1996) Class 3 Hox genes in insects and the origin of zen. Proc Natl Acad Sci USA 93: 8479–8484.

15. PanfilioKA, AkamM (2007) A comparison of Hox3 and Zen protein coding sequences in taxa that span the Hox3/zen divergence. Dev Genes Evol 217: 323–329.

16. Schmidt-Ott U, Rafiqi AM, Lemke S (2010) Hox3/zen and the Evolution of Extraembryonic Epithelia in Insects. In: Deutsch J, editor. Hox Genes Studies from the 20th to 21st Century: Springer New York. pp. 133–144.

17. ChaiCL, ZhangZ, HuangFF, WangXY, YuQY (2008) A genomewide survey of homeobox genes and identification of novel structure of the Hox cluster in the silkworm Bombyx mori. Insect Biochem Mol Biol 38: 1111–1120.

18. Heliconius GenomeC (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94–98.

19. ZhanS, MerlinC, BooreJL, ReppertSM (2011) The monarch butterfly genome yields insights into long-distance migration. Cell 147: 1171–1185.

20. XiaQ, ZhouZ, LuC, ChengD, DaiF, et al. (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science. 306: 1937–1940.

21. YouM, YueZ, HeW, YangX, YangG, et al. (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45: 220–225.

22. RegierJC, MitterC, ZwickA, BazinetAL, CummingsMP, et al. (2013) A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies). PLoS ONE 8: e58568.

23. RegierJC, ZwickA, CummingsMP, KawaharaAY, ChoS, et al. (2009) Toward reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evol Biol 9: 280.

24. KawaharaAY, BreinholtJW (2014) Phylogenomics provides strong evidence for relationships of butterflies and moths. P R Soc B 281: 20140970–20140970.

25. Grimaldi D (2005) Evolution of the Insects: Cambridge University Press. 755 p.

26. WahlbergN, WheatCW, PeñaC (2013) Timing and Patterns in the Taxonomic Diversification of Lepidoptera (Butterflies and Moths). PLoS ONE 8: e80875.

27. PanfilioKA, LiuPZ, AkamM, KaufmanTC (2006) Oncopeltus fasciatus zen is essential for serosal tissue function in katatrepsis. Dev Biol 292: 226–243.

28. SlatteryM, RileyT, LiuP, AbeN, Gomez-AlcalaP, et al. (2011) Cofactor Binding Evokes Latent Differences in DNA Binding Specificity between Hox Proteins. Cell 147: 1270–1282.

29. MannRS, LelliKM, JoshiR (2009) Hox specificity unique roles for cofactors and collaborators. Curr Top Dev Biol 88: 63–101.

30. KobayashiY, TanakaM, & AndoH (2003) Embryology. In Handbook of Zoology: Lepidoptera, Moths and Butterflies. Volume 2: Morphology, Physiology and Development 495–544. Kristensen, N.P. (Ed).

31. CarterJ-M, BakerSC, PinkR, CarterDR, CollinsA, et al. (2013) Unscrambling butterfly oogenesis. BMC Genomics 14: 283.

32. Nagy LM (2006) A summary of lepidopteran embryogenesis and experimental embryology. In: Goldsmith MR, Wilkins AS, editors. Molecular Model Systems in the Lepidoptera: Cambridge University Press.

33. KeinoH, TakesueS (1982) Scanning Electron microscopic Study on the Early Development of Silkworm Eggs (Bombyx mori L.). Dev Growth Differ 24: 287–294.

34. DamenWG, TautzD (1998) A Hox class 3 orthologue from the spider Cupiennius salei is expressed in a Hox-gene-like fashion. Dev Genes Evol 208: 586–590.

35. PapillonD, TelfordMJ (2007) Evolution of Hox3 and ftz in arthropods: insights from the crustacean Daphnia pulex. Dev Genes Evol 217: 315–322.

36. RushlowC, DoyleH, HoeyT, LevineM (1987) Molecular characterization of the zerknüllt region of the Antennapedia gene complex in Drosophila. Genes Dev 1: 1268–1279.

37. RushlowC, FraschM, DoyleH, LevineM (1987) Maternal regulation of zerknüllt: a homoeobox gene controlling differentiation of dorsal tissues in Drosophila. Nature 330: 583–586.

38. Van der ZeeM, BernsN, RothS (2005) Distinct functions of the Tribolium zerknüllt genes in serosa specification and dorsal closure. Curr Biol 15: 624–636.

39. StauberM, PrellA, Schmidt-OttU (2002) A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc Natl Acad Sci U S A 99: 274–279.

40. HughesCL, LiuPZ, KaufmanTC (2004) Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol Dev 6: 393–401.

41. DeardenP, GrbicM, FalcianiF, AkamM (2000) Maternal expression and early zygotic regulation of the Hox3/zen gene in the grasshopper Schistocerca gregaria. Evol Dev 2: 261–270.

42. Miya K (2003) The early embryonic development of Bombyx mori: an ultrastructural point of view. In: Yaginuma T, Suzuki K, editors: Gendaitosho. pp. 218.

43. LamerA, DornA (2001) The serosa of Manduca sexta (Insecta, Lepidoptera): ontogeny, secretory activity, structural changes, and functional considerations. Tissue and Cell 33: 580–595.

44. JacobsCGC, RezendeGL, LamersGEM, van der ZeeM (2013) The extraembryonic serosa protects the insect egg against desiccation. P R Soc B 280: 20131082–20131082.

45. PanfilioKA (2008) Extraembryonic development in insects and the acrobatics of blastokinesis. Dev Biol 313: 471–491.

46. ZraketCA, BarthJL, HeckelDG, AbbottAG (1990) Genetic Linkage Mapping with Restriction Fragment Length Polymorphisms in the Tobacco Budworm, Heliothis virescens. Molecular Insect Science 13–20.

47. ZerbinoDR, BirneyE (2008) Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

48. SimpsonJT, WongK, JackmanSD, ScheinJE, JonesSJM, et al. (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19: 1117–1123.

49. LiH (2012) Exploring single-sample SNP and INDEL calling with whole-genome de novo assembly. Bioinformatics 28: 1838–1844.

50. MarçaisG, KingsfordC (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27: 764–770.

51. PapadopoulosJS, AgarwalaR (2007) COBALT: constraint-based alignment tool for multiple protein sequences. Bioinformatics 23: 1073–1079.

52. StamatakisA, AlachiotisN (2010) Time and memory efficient likelihood-based tree searches on phylogenomic alignments with missing data. Bioinformatics 26: i132–139.

53. LartillotN, LepageT, BlanquartS (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286–2288.

54. YangZ (2007) PAML 4: Phylogenetic Analysis by Maximum Likelihood. Mol Biol Evol. 24: 1586–1591.

55. BrakefieldPM, BeldadeP, ZwaanBJ (2009) Fixation and dissection of embryos from the African butterfly Bicyclus anynana. Cold Spring Harbor Protocols 2009: pdb.prot5206–pdb.prot5206.

56. EswarN, WebbB, Marti-RenomMA, MadhusudhanMS, EramianD, et al. (2007) Comparative protein structure modeling using MODELLER. Curr Protoc Protein Sci Chapter 2: Unit 2.9–2.9.31.

57. FraenkelE, PaboCO (1998) Comparison of X-ray and NMR structures for the Antennapedia homeodomain-DNA complex. Nat Struct Biol 5: 692–697.

58. Leaver-FayA, TykaM, LewisSM, LangeOF, ThompsonJ, et al. (2011) ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Meth Enzymol 487: 545–574.

59. XuB, SchonesDE, WangY, LiangH, LiG (2013) A structural-based strategy for recognition of transcription factor binding sites. PLoS ONE 8: e52460.

60. PettersenEF, GoddardTD, HuangCC, CouchGS, GreenblattDM, et al. (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612.

Štítky
Genetika Reprodukčná medicína

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PLOS Genetics


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