Development Genes and Evolution

, Volume 217, Issue 6, pp 435–447 | Cite as

Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I

  • Kariena K. Dill
  • Katrin Thamm
  • Elaine C. Seaver
Original Article

Abstract

To investigate the evolutionary history of mesoderm in the bilaterian lineage, we are studying mesoderm development in the polychaete annelid, Capitella sp. I, a representative lophotrochozoan. In this study, we focus on the Twist and Snail families as candidate mesodermal patterning genes and report the isolation and in situ expression patterns of two twist homologs (CapI-twt1 and CapI-twt2) and two snail homologs (CapI-sna1 and CapI-sna2) in Capitella sp. I. CapI-twt1 is expressed in a subset of mesoderm derivatives during larval development, while CapI-twt2 shows more general mesoderm expression at the same stages. Neither twist gene is detected before the completion of gastrulation. The two snail genes have very distinct expression patterns. At cleavage and early gastrula stages, CapI-sna1 is broadly expressed in precursors of all three germ layers and becomes restricted to cells around the closing blastopore during late gastrulation; CapI-sna2 expression is not detected at these stages. After gastrulation, both snail genes are expressed in the developing central nervous system (CNS) at stages when neural precursor cells are internalized, and CapI-sna1 is also expressed laterally within the segmental mesoderm. Based on the expression patterns in this study, we suggest a putative function for Capitella sp. I twist genes in mesoderm differentiation and for snail genes in regulating CNS development and general cell migration during gastrulation.

Keywords

Capitella sp. I twist snail Spiralian mesoderm Polychaete 

Supplementary material

427_2007_153_Fig1_ESM.gif (15 kb)
Fig. S1

(A) Predicted amino acid sequences of the basic helix-loop-helix domains and WR motifs of CapI-Twt1 and CapI-Twt2 aligned with the corresponding domains of Twist homologs from other species. Consensus residues (as defined in Castanon and Baylies, 2002) for the ‘twist type’ basic helix-loop-helix domain and for the WR motif are shown in the bottom line of the alignment. (B) Predicted amino acid sequences of the 5 zinc-finger domains of CapI-Sna1 and CapI-Sna2 and the SNAG domain of CapI-Sna1 aligned with the corresponding domains of Snail homologs from other species. The first zinc-finger domain is not present in the human protein (Hs-sna) and the SNAG domain is not present in CapI-Sna2. Snail consensus residues in the zinc-finger sequences are shown in the bottom line of the alignment, shaded residues in CapI-Sna1 and CapI-Sna2 sequences indicate residues that differ from the conserved sequence. In each alignment, amino acid identities are indicated as dashes. Species abbreviations are as follows: CapI, Capitella sp. I; Pv, Patella vulgata; Dm, Drosophila melanogaster; Xl, Xenopus laevis; Hs, Homo sapiens (GIF 14 kb)

427_2007_153_Fig2_ESM.gif (16 kb)
Fig. S2

Maximum likelihood consensus tree of the basic-helix-loop-helix domains of Twist family proteins from Capitella sp. I and other species. Also included are sequences of related basic-helix-loop-helix proteins, Paraxis and Hairy. Support values calculated from the maximum likelihood analysis are above the branches; values below 50 are not included. Species abbreviations are as follows: CapI, Capitella sp. I; Xl, Xenopus laevis; Ec, Enchytraeus coronatus (oligochaete) ; Am, Apis Mellifera (honey bee); Dm, Drosophila melanogaster; Io, Ilynassa obsoleta (snail); HRO, Helobdella robusta (leech); Tt, Transennella tantilla (bivalve); Dr, Danio rerio; Pv, Patella vulgata (limpet); Gg, Gallus gallus; Hs, Homo sapiens; Mm, Mus musculus; Tc, Tribolium castaneum (beetle); Nv, Nematostella vectensis (sea anemone); Pc, Podocoryne carnea, (jellyfish) (GIF 16 kb)

427_2007_153_Fig3_ESM.gif (16 kb)
Fig. S3

Bayesian inference consensus tree of Snail and Slug family members from Capitella sp. I and other representative species. Sequences of Kruppel, a related zinc-finger protein, are included as an outgroup. Posterior probabilities from Bayesian analysis are reported above the branches and support values calculated from Maximum Likelihood analysis are below the branches; values below 50 are not included. Capitella sp. I genes are indicated with shaded boxes. Among the Snail family, lophotrochozoan genes are in purple and vertebrate genes are in green; the Scratch family is in blue. The two Capitella sp. I scratch genes included in the orthology analyses were isolated by degenerate PCR and RACE during our initial attempts at isolating snail fragments (Thamm and Seaver, unpublished). Species abbreviations are as follows: Hs, Homo sapiens; Mm, Mus musculus; Dr, Danio rerio; Gg, Gallus gallus; Xl, Xenopus laevis; CapI, Capitella sp. I; Pv, Patella vulgata (limpet); Nv, Nematostella vectensis (sea anemone); Am, Acropora millepora (coral); Pc, Podocoryne carnea, (jellyfish); HRO, Helobdella robusta (leech); Bf, Branchiostoma floridae (amphioxus); At, Achaearanea tepidariorum (spider); Dm, Drosophila melanogaster; Tc, Tribolium castaneum (beetle); Lf, Lithobius forficatus (centipede); Io, Ilynassa obsoleta (snail) (GIF 15 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105PubMedCrossRefGoogle Scholar
  2. Alberga A, Boulay JL, Kempe E, Dennefeld C, Haenlin M (1991) The snail gene required for mesoderm formation in Drosophila is expressed dynamically in derivatives of all three germ layers. Development 111:983–992PubMedGoogle Scholar
  3. Anderson DT (1973) Embryology and phylogeny in Annelids and Arthropods. Pergamon, OxfordGoogle Scholar
  4. Ashraf SI, Ip YT (2001) The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128:4757–4767PubMedGoogle Scholar
  5. Ashraf SI, Hu X, Roote J, Ip YT (1999) The mesoderm determinant snail collaborates with related zinc-finger proteins to control Drosophila neurogenesis. EMBO J 18:6426–6438PubMedCrossRefGoogle Scholar
  6. Barrallo-Gimeno A, Nieto MA (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132:3151–3161PubMedCrossRefGoogle Scholar
  7. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J, Garcia De Herreros A (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2:84–89PubMedCrossRefGoogle Scholar
  8. Baylies MK, Bate M (1996) twist: a myogenic switch in Drosophila. Science 272:1481–1484PubMedCrossRefGoogle Scholar
  9. Bhup R, Marsden JR (1981) The development of the central nervous system in Capitella capitata (Polychaeta, Annelida). Can J Zool 60:2284–2295CrossRefGoogle Scholar
  10. Cai Y, Chia W, Yang X (2001) A family of snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. EMBO J 20:1704–1714PubMedCrossRefGoogle Scholar
  11. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76–83PubMedCrossRefGoogle Scholar
  12. Castanon I, Baylies MK (2002) A Twist in fate: evolutionary comparison of Twist structure and function. Gene 287:11–22PubMedCrossRefGoogle Scholar
  13. Cripps RM, Black BL, Zhao B, Lien CL, Schulz RA, Olson EN (1998) The myogenic regulatory gene Mef2 is a direct target for transcriptional activation by Twist during Drosophila myogenesis. Genes Dev 12:422–434PubMedGoogle Scholar
  14. Dohle W, Gerberding M, Hejnol A, Scholtz G (2004) Cell lineage, segment differentiation, and gene expression in crustaceans. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Sweets and Zeitlinger, Lisse, The Netherlands, pp 95–133Google Scholar
  15. Eckelbarger KJ, Linley PA, Grassle JP (1984) Role of ovarian follicle cells in vitellogenesis and oocyte resorption in Capitella sp. I (Polychaeta). Mar Biol 79:133–144CrossRefGoogle Scholar
  16. Eisig H (1899) Zur Entwicklungsgeschichte der Capitelliden. Mittheilungen Aus der Zoologischen Station Zu Neapel 13:5–39Google Scholar
  17. Frobius AC, Seaver EC (2006) Capitella sp. I homeobrain-like, the first lophotrochozoan member of a novel paired-like homeobox gene family. Gene Expr Patterns 6:985–991PubMedCrossRefGoogle Scholar
  18. Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801PubMedCrossRefGoogle Scholar
  19. Goldstein B, Leviten MW, Weisblat DA (2001) Dorsal and snail homologs in leech development. Dev Genes Evol 211:329–337PubMedCrossRefGoogle Scholar
  20. Grassle JP, Grassle JF (1976) Sibling species in the marine polution indicator Capitella (Polychaeta). Science 192:567–569PubMedCrossRefGoogle Scholar
  21. Grau Y, Carteret C, Simpson P (1984) Mutations and chromosomal rearrangements affecting the expression of snail, a gene involved in embryonic patternin in Drosophila melanogaster. Genetics 108:347–360PubMedGoogle Scholar
  22. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  23. Handel K, Basal A, Fan X, Roth S (2005) Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle. Dev Genes Evol 215:13–31PubMedCrossRefGoogle Scholar
  24. Harfe BD, Vaz Gomes A, Kenyon C, Liu J, Krause M, Fire A (1998) Analysis of a Caenorhabditis elegans Twist homolog identifies conserved and divergent aspects of mesodermal patterning. Genes Dev 12:2623–2635PubMedGoogle Scholar
  25. Hopwood ND, Pluck A, Gurdon JB (1989) A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59:893–903PubMedCrossRefGoogle Scholar
  26. Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  27. Langeland JA, Tomsa JM, Jackman WR Jr, Kimmel CB (1998) An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev Genes Evol 208:569–577PubMedCrossRefGoogle Scholar
  28. Leptin M (1991) twist and snail as positive and negative regulators during Drosophila mesoderm development. Genes Dev 5:1568–1576PubMedGoogle Scholar
  29. Lespinet O, Nederbragt AJ, Cassan M, Dictus WJ, van Loon AE, Adoutte A (2002) Characterisation of two snail genes in the gastropod mollusc Patella vulgata. Implications for understanding the ancestral function of the snail-related genes in Bilateria. Dev Genes Evol 212:186–195PubMedCrossRefGoogle Scholar
  30. Mayor R, Essex LJ, Bennett MF, Sargent MG (1993) Distinct elements of the xsna promoter are required for mesodermal and ectodermal expression. Development 119:661–671PubMedGoogle Scholar
  31. Nederbragt AJ, Lespinet O, van Wageningen S, van Loon AE, Adoutte A, Dictus WJ (2002) A lophotrochozoan twist gene is expressed in the ectomesoderm of the gastropod mollusk Patella vulgata. Evol Dev 4:334–343PubMedCrossRefGoogle Scholar
  32. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155–166PubMedCrossRefGoogle Scholar
  33. Nieto MA, Bennett MF, Sargent MG, Wilkinson DG (1992) Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 116:227–237PubMedGoogle Scholar
  34. Nieto MA, Sargent MG, Wilkinson DG, Cooke J (1994) Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264:835–839PubMedCrossRefGoogle Scholar
  35. Nusslein-Volhard C, Weischaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Wilheim Roux Arch Dev Biol 193:267–282CrossRefGoogle Scholar
  36. Perez-Pomares JM, Munoz-Chapuli R (2002) Epithelial-mesenchymal transitions: a mesodermal cell strategy for evolutive innovation in Metazoans. Anat Rec 268:343–351PubMedCrossRefGoogle Scholar
  37. Pioro HL, Stollewerk A (2006) The expression pattern of genes involved in early neurogenesis suggests distinct and conserved functions in the diplopod Glomeris marginata. Dev Genes Evol 216:417–430PubMedCrossRefGoogle Scholar
  38. Price AL, Patel NH (2007) Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. J Exp Zoolog B Mol Dev Evol (in press)Google Scholar
  39. Ruppert E, Barnes R (1994) Invertebrate zoology. Thomson learning, BelmontGoogle Scholar
  40. Sargent MG, Bennett MF (1990) Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development 109:967–973PubMedGoogle Scholar
  41. Saulnier-Michel C (1992) Polychaeta: Digestive system. Wiley-Liss, New YorkGoogle Scholar
  42. Seaver EC, Kaneshige LM (2006) Expression of ‘segmentation’ genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol 289:179–194PubMedCrossRefGoogle Scholar
  43. Seaver EC, Paulson DA, Irvine SQ, Martindale MQ (2001) The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. Dev Biol 236:195–209PubMedCrossRefGoogle Scholar
  44. Seaver EC, Thamm K, Hill SD (2005) Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 7:312–326PubMedCrossRefGoogle Scholar
  45. Simpson P (1983) Maternal-zygotic gene interactions during formation of the dorsoventral pattern in Drosophila embryos. Genetics 105:615–632PubMedGoogle Scholar
  46. Smith DE, Franco del Amo F, Gridley T (1992) Isolation of Sna, a mouse gene homologous to the Drosophila genes snail and escargot: its expression pattern suggests multiple roles during postimplantation development. Development 116:1033–1039PubMedGoogle Scholar
  47. Sommer RJ, Tautz D (1994) Expression patterns of twist and snail in Tribolium (Coleoptera) suggest a homologous formation of mesoderm in long and short germ band insects. Dev Genet 15:32–37PubMedCrossRefGoogle Scholar
  48. Swofford DL (2000) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Sinauer, Sunderland, MAGoogle Scholar
  49. Tavares AT, Izpisuja-Belmonte JC, Rodriguez-Leon J (2001) Developmental expression of chick twist and its regulation during limb patterning. Int J Dev Biol 45:707–713PubMedGoogle Scholar
  50. Technau U, Scholz CB (2003) Origin and evolution of endoderm and mesoderm. Int J Dev Biol 47:531–539PubMedGoogle Scholar
  51. Thisse B, Stoetzel C, Gorostiza-Thisse C, Perrin-Schmitt F (1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7:2175–2183PubMedGoogle Scholar
  52. Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203–1215PubMedGoogle Scholar
  53. Thisse C, Thisse B, Postlethwait JH (1995) Expression of snail2, a second member of the zebrafish snail family, in cephalic mesendoderm and presumptive neural crest of wild-type and spadetail mutant embryos. Dev Biol 172:86–99PubMedCrossRefGoogle Scholar
  54. Wada S, Saiga H (1999) Cloning and embryonic expression of Hrsna, a snail family gene of the ascidian Halocynthia roretzi: implication in the origins of mechanisms for mesoderm specification and body axis formation in chordates. Dev Growth Differ 41:9–18PubMedCrossRefGoogle Scholar
  55. Wang SM, Coljee VW, Pignolo RJ, Rotenberg MO, Cristofalo VJ, Sierra F (1997) Cloning of the human twist gene: its expression is retained in adult mesodermally derived tissues. Gene 187:83–92PubMedCrossRefGoogle Scholar
  56. Weller M, Tautz D (2003) Prospero and Snail expression during spider neurogenesis. Dev Genes Evol 213:554–566PubMedCrossRefGoogle Scholar
  57. Werbrock AH, Meiklejohn DA, Sainz A, Iwasa JH, Savage RM (2001) A polychaete hunchback ortholog. Dev Biol 235:476–488PubMedCrossRefGoogle Scholar
  58. Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F (1991) The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol 143:363–373PubMedCrossRefGoogle Scholar
  59. Yasui K, Zhang SC, Uemura M, Aizawa S, Ueki T (1998) Expression of a twist-related gene, Bbtwist, during the development of a lancelet species and its relation to cephalochordate anterior structures. Dev Biol 195:49–59PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Kariena K. Dill
    • 1
  • Katrin Thamm
    • 1
  • Elaine C. Seaver
    • 1
  1. 1.Kewalo Marine Laboratory, Pacific Biosciences Research CenterUniversity of HawaiiHonoluluUSA

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