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

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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.

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Acknowledgements

The Capitella sp. I genomic and EST sequence data were produced by the US Department of Energy Joint Genome Institute (http://www.jgi.doe.gov/). We thank lab members Néva Meyer and Michael Boyle for sharing unpublished data and commenting on this manuscript, and Lori Kaneshige for assistance with preliminary in situ experiments. We also thank David Matus for assistance with gene orthology analyses and two anonymous reviewers for insightful comments. This work was supported by NSF grants IOB05-44869 and EF0531558.

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  1. Katrin Thamm

    Present address: Institut für Allgemeine und Spezielle Zoologie, Abteilung Entwicklungsbiologie, Justus-Liebig-Universität Gießen, Stephanstraße 24, 35390, Gießen, Germany

Authors and Affiliations

  1. Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii, 41 Ahui Street, Honolulu, HI, 96813, USA

    Kariena K. Dill, Katrin Thamm & Elaine C. Seaver

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  1. Kariena K. Dill
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Correspondence to Elaine C. Seaver.

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Communicated by D.A. Weisblat

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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_Fig1_ESM.tif

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_Fig2_ESM.tif

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)

427_2007_153_Fig3_ESM.tif

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Dill, K.K., Thamm, K. & Seaver, E.C. Characterization of twist and snail gene expression during mesoderm and nervous system development in the polychaete annelid Capitella sp. I. Dev Genes Evol 217, 435–447 (2007). https://doi.org/10.1007/s00427-007-0153-4

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