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Localization of Vasa mRNA during early cleavage of the snail Ilyanassa

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Abstract

Members of the Vasa family of helicases are specifically localized to germ line lineages in embryos of many animal groups and, in some cases, have been shown to be required for germ line formation. Despite considerable attention to the embryology of gastropod molluscs, the germ line has not been identified in the early cleavage stages of these embryos. We have cloned a Vasa ortholog in the snail Ilyanassa and examined the distribution of IoVasa mRNA during early cleavage. Initially, the transcript is present in all cells and non-specifically localized to centrosomes in a subset of cells. The IoVasa mRNA becomes progressively more enriched in the dorsal quadrant of the embryo, and then becomes restricted to particular cells in the 4d lineage. At the 64-cell stage, IoVasa mRNA is detected in 4dL11, 4dL12, 4dR11, and 4dR12. Following another round of division in the 4d lineage, the mRNA is restricted to two cells: 4dL121 and 4dR121. By the 108-cell stage, IoVasa mRNA is no longer detectable. Because the germ line is thought to arise from the 4d lineage in spiralians, these data are consistent with the hypothesis that the Ilyanassa germ line is marked by inheritance of IoVasa and derived from the cells 4dL121 and 4dR121. Alternatively, IoVasa may be required in somatic lineages where it is expressed, and the germ line may be specified later in development.

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References

  • Conklin EG (1897) The embryology of crepidula, a contribution to the cell lineage and early development of some marine gasteropods. J Morphol 13:1–226

    Article  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  PubMed  CAS  Google Scholar 

  • Fabioux C, Huvet A, Lelong C, Robert R, Pouvreau S, Daniel JY, Minguant C, Le Pennec M (2004) Oyster vasa-like gene as a marker of the germ line cell development in Crassostrea gigas. Biochem Biophys Res Commun 320:592–598

    Article  PubMed  CAS  Google Scholar 

  • Gavis ER, Lunsford L, Bergsten SE, Lehmann R (1996) A conserved 90 nucleotide element mediates translational repression of nanos RNA. Development 122:2791–2800

    PubMed  CAS  Google Scholar 

  • Goulding M (2001) Comparative and experimental analysis of precocious cell-lineage diversification in the embryonic dorsoventral axis of the gastropod Ilyanassa. Ph.D. thesis, Zoology Department, University of Texas, Austin

    Google Scholar 

  • Griffond B (1977) Individualization and organogenesis of embryonic gonad in gonochoric prosobranch mollusk Viviparus viviparus (L.). Roux Arch Dev Biol 183:131–147

    Article  Google Scholar 

  • Halanych KM (2004) The new view of animal phylogeny. Ann Rev Ecolog Evol Syst 35:229–256

    Article  Google Scholar 

  • Hay B, Jan LY, Jan YN (1988) A protein-component of Drosophila polar granules is encoded by vasa and has extensive sequence similarity to ATP-dependent helicases. Cell 55:577–587

    Article  PubMed  CAS  Google Scholar 

  • Henry JJ, Martindale MQ (1998) Conservation of the spiralian developmental program: cell lineage of the nemertean, Cerebratulus lacteus. Dev Biol 201:253–269

    Article  PubMed  CAS  Google Scholar 

  • Henry JQ, Tagawa K, Martindale MQ (2001) Deuterostome evolution: early development in the enteropneust hemichordate, Ptychodera flava. Evol Dev 3:375–390

    Article  PubMed  CAS  Google Scholar 

  • Kang D, Pilon M, Weisblat DA (2002) Maternal and zygotic expression of a nanos-class gene in the leech Helobdella robusta: primordial germ cells arise from segmental mesoderm. Dev Biol 245:28–41

    Article  PubMed  CAS  Google Scholar 

  • Kingsley EP, Chan XY, Duan Y, Lambert JD (2007) Widespread RNA segregation in a spiralian embryo. Evol Dev 9:527–539

    Article  PubMed  CAS  Google Scholar 

  • Kuznicki KA, Smith PA, Leung-Chiu WMA, Estevez AO, Scott HC, Bennett KL (2000) Combinatorial RNA interference indicates GLH-4 can compensate for GLH-1; these two P granule components are critical for fertility in C-elegans. Development 127:2907–2916

    PubMed  CAS  Google Scholar 

  • Lambert JD (2008) Mesoderm in spiralians: the organizer and the 4d cell. J Exp Zoolog B Mol Dev Evol 310B:15–23

    Article  Google Scholar 

  • Lambert JD, Nagy LM (2002) Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 420:682–686

    Article  PubMed  CAS  Google Scholar 

  • Lasko PF, Ashburner M (1988) The product of the Drosophila gene vasa is very similar to eukaryotic initiation factor-4A. Nature 335:611–617

    Article  PubMed  CAS  Google Scholar 

  • Rebscher N, Zelada-Gonzalez F, Banisch TU, Raible F, Arendt D (2007) Vasa unveils a common origin of germ cells and of somatic stem cells from the posterior growth zone in the polychaete Platynereis dumerilii. Dev Biol 306:599–611

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Schupbach T, Wieschaus E (1986) Germ line autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev Biol 113:443–448

    Article  PubMed  CAS  Google Scholar 

  • Styhler S, Nakamura A, Swan A, Suter B, Lasko P (1998) Vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germ line cyst development. Development 125:1569–1578

    PubMed  CAS  Google Scholar 

  • Tadokoro R, Sugio M, Kutsuna J, Tochinai S, Takahashi Y (2006) Early segregation of germ and somatic lineages during gonadal regeneration in the annelid Enchytraeus japonensis. Curr Biol 16:1012–1017

    Article  PubMed  CAS  Google Scholar 

  • Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T (2000) The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Gene Dev 14:841–853

    PubMed  CAS  Google Scholar 

  • Tomancak P, Guichet A, Zavorszky P, Ephrussi A (1998) Oocyte polarity depends on regulation of gurken by Vasa. Development 125:1723–1732

    PubMed  CAS  Google Scholar 

  • Vagin VV, Klenov MS, Kalmykova AI, Stolyarenko AD, Kotelnikov RN, Gvozdev VA (2004) The RNA interference proteins and vasa locus are involved in the silencing of retrotransposons in the female germ line of Drosophila melanogaster. RNA Biol 1:54–58

    PubMed  CAS  Google Scholar 

  • Wang Y, Zayas RM, Guo T, Newmark PA (2007) nanos function is essential for development and regeneration of planarian germ cells. Proc Natl Acad Sci U S A 104:5901–5906

    Article  PubMed  CAS  Google Scholar 

  • Woods FH (1931) History of the germ cells in Sphaerium striatinum. J Morphol Physiol 51:545–595

    Article  Google Scholar 

  • Woods FH (1932) Keimbahn determinants and continuity of the germ cells in Sphaerium striatinum (Lam.). J Morphol Physiol 53:345–265

    Article  Google Scholar 

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Acknowledgements

We thank M. Goulding for sharing diagrams of cell position during Ilyanassa gastrulation and comments on the manuscript, R. Glor for advice on phylogenetic reconstruction, and J. Rabinowitz for useful advice and for comments on the manuscript. This work was funded in part by a National Science Foundation grant (IOB0544220) to J.D. Lambert.

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Correspondence to J. David Lambert.

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Communicated by D.A. Weisblat

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Swartz, S.Z., Chan, X.Y. & Lambert, J.D. Localization of Vasa mRNA during early cleavage of the snail Ilyanassa . Dev Genes Evol 218, 107–113 (2008). https://doi.org/10.1007/s00427-008-0203-6

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  • DOI: https://doi.org/10.1007/s00427-008-0203-6

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