Snakes: Hatching of a model system for Evo-Devo?

International Journal of Developmental Biology

Volumn 58, Issue 10-12, 2014, Pages 727-732

  Guerreiro, Isabel ^a   Duboule, Denis ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b EPFL   (Switzerland)

Author keywords

Axial extension; Hox gene; Model organism; Snake; Vertebrae

Indexed keywords

AMNIOTE; ANIMAL EMBRYO; ARTICLE; BURROWING SPECIES; DEVELOPMENTAL BIOLOGY; EMBRYO DEVELOPMENT; EMBRYO SEGMENTATION; EVOLUTION; EVOLUTIONARY ADAPTATION; GENE EXPRESSION; HATCHING; HOX GENE; LIZARD; NEXT GENERATION SEQUENCING; NONHUMAN; ORGAN SIZE; PRIORITY JOURNAL; SNAKE; THORAX; TRANSCRIPTION REGULATION; ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; EMBRYOLOGY; GENETICS; GENOME; HOMEOBOX; NONMAMMALIAN EMBRYO;

ANIMALIA; SERPENTES; VERTEBRATA;

ANIMALS; BIOLOGICAL EVOLUTION; EMBRYO, NONMAMMALIAN; GENES, HOMEOBOX; GENOME; MODELS, ANIMAL; MODELS, BIOLOGICAL; SNAKES;

EID: 84936772889     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.150026dd     Document Type: Article

References (62)

1. ALFOLDI, J., DI PALMA, F., GRABHERR, M., WILLIAMS, C., KONG, L., MAUCELI, E., RUSSELL, P., LOWE, C.B., GLOR, R.E., JAFFE, J.D. et al., (2011). The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477: 587-591.
2. ARNOULT, L., SU, K.F., MANOEL, D., MINERVINO, C., MAGRINA, J., GOMPEL, N. and PRUD'HOMME, B. (2013). Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339: 1423-1426.
3. BARTON, S.C., SURANI, M.A. and NORRIS, M.L. (1984). Role of paternal and maternal genomes in mouse development. Nature 311: 374-376.
4. CARROLL, S.B. (2005). Evolution at two levels: on genes and form. PLoS Biol 3: e245.
5. CASTOE, T.A., BRAUN, E.L., BRONIKOWSKI, A.M., COX, C.L., RABOSKY, A.R., JASON DE KONING, A.P., DOBRY, J., FUJITA, M.K., GIORGIANNI, M.W., HARGREAVES, A. et al., (2012). Report from the first snake genomics and integrative biology meeting. Stand Genomic Sci 7: 150-152.
6. CASTOE, T.A., DE KONING, A.P., HALL, K.T., CARD, D.C., SCHIELD, D.R., FUJITA, M.K., RUGGIERO, R.P., DEGNER, J.F., DAZA, J.M., GU, W. et al., (2013). The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proc Natl Acad Sci USA 110: 20645-20650.
7. CHENG, Y., MA, Z., KIM, B.H., WU, W., CAYTING, P., BOYLE, A.P., SUNDARAM, V., XING, X., DOGAN, N., LI, J. et al., (2014). Principles of regulatory information conservation between mouse and human. Nature 515: 371-375.
8. COHN, M.J. and TICKLE, C. (1999). Developmental basis of limblessness and axial patterning in snakes. Nature 399: 474-479.
9. COOPER, K.L., SEARS, K.E., UYGUR, A., MAIER, J., BACZKOWSKI, K.S., BROSNAHAN, M., ANTCZAK, D., SKIDMORE, J.A. and TABIN, C.J. (2014). Patterning and post-patterning modes of evolutionary digit loss in mammals. Nature 511: 41-45.
10. DE ROBERTIS, E.M. (2008). Evo-devo: variations on ancestral themes. Cell 132: 185-195.
11. DI-POÏ, N., MONTOYA-BURGOS, J.I. and DUBOULE, D. (2009). Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard. Genome Res. 19: 602-610.
12. DI-POI, N., MONTOYA-BURGOS, J.I., MILLER, H., POURQUIE, O., MILINKOVITCH, M.C. and DUBOULE, D. (2010). Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 464: 99-103.
13. DI-POÏ, N., MONTOYA-BURGOS, J.I., MILLER, H., POURQUIE, O., MILINKOVITCH, M.C. and DUBOULE, D. (2010). Changes in Hox genes' structure and function during the evolution of the squamate body plan. Nature 464: 99-103.
14. DUBOULE, D. (2005). Endless forms most beautiful - The new science of evo devo and the making of the animal kingdom. Science 308: 955-956.
15. DUBOULE, D. (2007). The rise and fall of Hox gene clusters. Development 134: 2549-2560.
16. DUBOULE, D. (2010). The evo-devo comet. EMBO reports 11: 489.
17. DUBOULE, D. and MORATA, G. (1994). Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10: 358-364.
18. FRY, B.G., VIDAL, N., NORMAN, J.A., VONK, F.J., SCHEIB, H., RAMJAN, S.F., KURUPPU, S., FUNG, K., HEDGES, S.B., RICHARDSON, M.K. et al., (2006). Early evolution of the venom system in lizards and snakes. Nature 439: 584-588.
19. GILBERT, C., MEIK, J.M., DASHEVSKY, D., CARD, D.C., CASTOE, T.A. and SCHAACK, S. (2014). Endogenous hepadnaviruses, bornaviruses and circoviruses in snakes. Proc Biol Sci 281: 20141122.
20. GOMEZ, C., OZBUDAK, E.M., WUNDERLICH, J., BAUMANN, D., LEWIS, J. and POURQUIE, O. (2008). Control of segment number in vertebrate embryos. Nature 454: 335-339.
21. GOMEZ, C. and POURQUIE, O. (2009). Developmental control of segment numbers in vertebrates. J Exp Zool B Mol Dev Evol 312: 533-544.
22. GREEN, R.E., BRAUN, E.L., ARMSTRONG, J., EARL, D., NGUYEN, N., HICKEY, G., VANDEWEGE, M.W., ST JOHN, J.A., CAPELLA-GUTIERREZ, S., CASTOE, T.A. et al., (2014). Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346: 1254449.
23. GUERREIRO, I., NUNES, A., WOLTERING, J.M., CASACA, A., NÓVOA, A., VINAGRE, T., HUNTER, M.E., DUBOULE, D. and MALLO, M. (2013). Role of a polymorphism in a Hox/Pax-responsive enhancer in the evolution of the vertebrate spine. Proc. Natl. Acad. Sci. USA 110: 10682-10686.
24. HARVEY, A.L. (2014). Toxins and drug discovery. Toxicon 92C: 193-200.
25. HEAD, J.J. and POLLY, P.D. (2015). Evolution of the snake body form reveals homoplasy in amniote Hox gene function. Nature 520: 86-89.
26. HELD I, L.J. (2014). How the Snake Lost its Legs: Curious Tales from the Frontier of Evo-Devo. Cambridge University Press.
27. HENGARTNER, M.O. and HORVITZ, H.R. (1994). C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell 76: 665-676.
28. KESSEL, M. and GRUSS, P. (1991). Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67: 89-104.
29. KMITA, M., FRAUDEAU, N., HERAULT, Y. and DUBOULE, D. (2002). Serial deletions and duplications suggest a mechanism for the collinearity of Hoxd genes in limbs. Nature 420: 145-150.
30. KOK, F.O., SHIN, M., NI, C., GUPTA, A., GROSSE, A.S., VAN IMPEL, A., KIRCHMAIER, B.C., PETERSON-MADURO, J., KOURKOULIS, G., MALE, I. et al., (2014). Reverse Genetic Screening Reveals Poor Correlation between Morpholino-Induced and Mutant Phenotypes in Zebrafish. Dev Cell 32: 97-108.
31. LE DOUARIN, N.M. (2004). The avian embryo as a model to study the development of the neural crest: a long and still ongoing story. Mech Dev 121: 1089-1102.
32. LEMAITRE, B., NICOLAS, E., MICHAUT, L., REICHHART, J.M. and HOFFMANN, J.A. (1996). The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973-983.
33. LEWIS, E.B. (1978). A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
34. LUTES, A.A., NEAVES, W.B., BAUMANN, D.P., WIEGRAEBE, W. and BAUMANN, P. (2010). Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464: 283-286.
35. MCGRATH, J. and SOLTER, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37: 179-183.
36. MCINTYRE, D.C., RAKSHIT, S., YALLOWITZ, A.R., LOKEN, L., JEANNOTTE, L., CAPECCHI, M.R. and WELLIK, D.M. (2007). Hox patterning of the vertebrate rib cage. Development 134: 2981-2989.
37. MENEZ, A., STOCKLIN, R. and MEBS, D. (2006). 'Venomics' or: The venomous systems genome project. Toxicon 47: 255-259.
38. MILINKOVITCH, M.C., MANUKYAN, L., DEBRY, A., DI-POI, N., MARTIN, S., SINGH, D., LAMBERT, D. and ZWICKER, M. (2013). Crocodile head scales are not developmental units but emerge from physical cracking. Science 339: 78-81.
39. MILINKOVITCH, M.C. and TZIKA, A. (2007). Escaping the mouse trap: the selection of new Evo-Devo model species. J Exp Zool B Mol Dev Evol 308: 337-346.
40. MURPHY, B.F. and THOMPSON, M.B. (2011). A review of the evolution of viviparity in squamate reptiles: the past, present and future role of molecular biology and genomics. J Comp Physiol B 181: 575-594.
41. NAGASHIMA, H., SUGAHARA, F., TAKECHI, M., ERICSSON, R., KAWASHIMA-OHYA, Y., NARITA, Y. and KURATANI, S. (2009). Evolution of the turtle body plan by the folding and creation of new muscle connections. Science 325: 193-196.
42. POURQUIE, O. (2003). The segmentation clock: converting embryonic time into spatial pattern. Science 301: 328-330.
43. SATOH, N. and LEVINE, M. (2005). Surfing with the tunicates into the post-genome era. Genes Dev 19: 2407-2411.
44. SCHWARTZ, T.S., TAE, H., YANG, Y., MOCKAITIS, K., VAN HEMERT, J.L., PROULX, S.R., CHOI, J.H. and BRONIKOWSKI, A.M. (2010). A garter snake transcriptome: pyrosequencing, de novo assembly, and sex-specific differences. BMC genomics 11: 694.
45. SHAFFER, H.B., MINX, P., WARREN, D.E., SHEDLOCK, A.M., THOMSON, R.C., VALENZUELA, N., ABRAMYAN, J., AMEMIYA, C.T., BADENHORST, D., BIGGAR, K.K. et al., (2013). The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14: R28.
46. SHINE, R. and BONNET, X. (2000). Snakes: a new 'model organism' in ecological research? Trends Ecol Evol 15: 221-222.
47. SIMONS, C., PHEASANT, M., MAKUNIN, I.V. and MATTICK, J.S. (2006). Transposon-free regions in mammalian genomes. Genome Res. 16: 164-172.
48. SMITH, K. and SPADAFORA, C. (2005). Sperm-mediated gene transfer: applications and implications. BioEssays 27: 551-562.
49. SOMMER, R.J. (2009). The future of evo-devo: model systems and evolutionary theory. Nat Rev Genet 10: 416-422.
50. STERGACHIS, A.B., NEPH, S., SANDSTROM, R., HAUGEN, E., REYNOLDS, A.P., ZHANG, M., BYRON, R., CANFIELD, T., STELHING-SUN, S., LEE, K. et al., (2014). Conservation of trans-acting circuitry during mammalian regulatory evolution. Nature 515: 365-70.
51. TABIN, C. and WOLPERT, L. (2007). Rethinking the proximodistal axis of the vertebrate limb in the molecular era. Genes Dev. 21: 1433-1442.
52. TZIKA, A. and MILINKOVITCH, M.C. (2008). A Pragmatic Approach for Selecting Evo-Devo Model Species in Amniotes. In Evolving Pathways; Key Themes in Evolutionary Developmental Biology, (ed. MINELLI, A. and FUSCO, G.). Cambridge University Press, Cambridge, pp.119-140.
53. TZIKA, A.C., HELAERS, R., SCHRAMM, G. and MILINKOVITCH, M.C. (2011). Reptilian-transcriptome v1.0, a glimpse in the brain transcriptome of five divergent Sauropsida lineages and the phylogenetic position of turtles. EvoDevo 2: 19.
54. VIDAL, N. and HEDGES, S.B. (2004). Molecular evidence for a terrestrial origin of snakes. Proc. Royal Soc. London B: Biol. Sci. 271: S226-S229.
55. VONK, F.J., CASEWELL, N.R., HENKEL, C.V., HEIMBERG, A.M., JANSEN, H.J., MCCLEARY, R.J.R., KERKKAMP, H.M.E., VOS, R.A., GUERREIRO, I., CALVETE, J.J. et al., (2013). The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proc. Natl. Acad. Sci. USA 110: 20651-20656.
56. WANG, Z., PASCUAL-ANAYA, J., ZADISSA, A., LI, W., NIIMURA, Y., HUANG, Z., LI, C., WHITE, S., XIONG, Z., FANG, D. et al., (2013). The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet 45: 701-706.
57. WELLIK, D.M. (2003). Hox10 and Hox11 Genes Are Required to Globally Pattern the Mammalian Skeleton. Science 301: 363-367.
58. WOLTERING, J.M. (2012). From lizard to snake; behind the evolution of an extreme body plan. Curr. Genomics 13: 289-299.
59. WOLTERING, J.M., VONK, F.J., MÜLLER, H., BARDINE, N., TUDUCE, I.L., DE BAKKER, M.A.G., KNÖCHEL, W., SIRBU, I.O., DURSTON, A.J. and RICHARDSON, M.K. (2009). Axial patterning in snakes and caecilians: Evidence for an alternative interpretation of the Hox code. Dev. Biol. 332: 82-89.
60. YOUNG, T. and DESCHAMPS, J. (2009). Hox, Cdx, and anteroposterior patterning in the mouse embryo. Curr Top Dev Biol 88: 235-255.
61. YOUNG, T., ROWLAND, J.E., VAN DE VEN, C., BIALECKA, M., NOVOA, A., CARAPUCO, M., VAN NES, J., DE GRAAFF, W., DULUC, I., FREUND, J.-N. et al., (2009). Cdx and Hox genes differentially regulate posterior axial growth in mammalian embryos. Developmental Cell 17: 516-526.
62. YUE, F.CHENG, Y.BRESCHI, A.VIERSTRA, J.WU, W.RYBA, T.SANDSTROM, R.MA, Z.DAVIS, C.POPE, B.D. et al., (2014). A comparative encyclopedia of DNA elements in the mouse genome. Nature 515: 355-364.