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The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration

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Abstract

Planarians are highly regenerative organisms with the ability to remake all their cell types, including the germ cells. The germ cells have been suggested to arise from totipotent neoblasts through epigenetic mechanisms. Nanos is a zinc-finger protein with a widely conserved role in the maintenance of germ cell identity. In this work, we describe the expression of a planarian nanos-like gene Smednos in two kinds of precursor cells namely, primordial germ cells and eye precursor cells, during both development and regeneration of the planarian Schmidtea mediterranea. In sexual planarians, Smednos is expressed in presumptive male primordial germ cells of embryos from stage 8 of embryogenesis and throughout development of the male gonads and in the female primordial germ cells of the ovary. Thus, upon hatching, juvenile planarians do possess primordial germ cells. In the asexual strain, Smednos is expressed in presumptive male and female primordial germ cells. During regeneration, Smednos expression is maintained in the primordial germ cells, and new clusters of Smednos-positive cells appear in the regenerated tissue. Remarkably, during the final stages of development (stage 8 of embryogenesis) and during regeneration of the planarian eye, Smednos is expressed in cells surrounding the differentiating eye cells, possibly corresponding to eye precursor cells. Our results suggest that similar genetic mechanisms might be used to control the differentiation of precursor cells during development and regeneration in planarians.

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References

  • Baguñà J, Saló E, Auladell C (1989) Regeneration and pattern formation in planarians. III. Evidence that neoblasts are totipotent stem cells and the source of blastema cells. Development 107:77–86

    Google Scholar 

  • Benazzi M, Baguñà J, Ballester R, Puccinelli I, del Papa R (1975) Further contribution to the taxonomy of the Dugesia lugubris-polychroa group with description of Dugesia mediterranea n.sp. (Tricladida, Paludicola). Boll Zool 42:81–89

    Google Scholar 

  • Cardona A, Hartenstein V, Romero R (2005a) The embryonic development of the triclad Schmidtea polychroa. Dev Genes Evol 215:109–131

    Article  PubMed  Google Scholar 

  • Cardona A, Fernández J, Solana J, Romero R (2005b) An in situ hybridization protocol for planarian embryos: monitoring myosin heavy chain gene expression. Dev Genes Evol 215:482–488

    Article  PubMed  Google Scholar 

  • Cebrià F, Bueno D, Reigada S, Romero R (1999) Intercalary muscle cell renewal in planarian pharynx. Dev Genes Evol 209:249–253

    Article  PubMed  Google Scholar 

  • Cebrià F, Newmark PA (2005) Planarian homologs of netrin and netrin receptor are required for proper regeneration of the central nervous system and the maintenance of nervous system architecture. Development 132:3691–3703

    Article  PubMed  Google Scholar 

  • Curtis WC (1902) The life history, the normal fission, and the reproductive organs of Planaria maculata. Proc Boston Soc Nat Hist 30:515–559

    Google Scholar 

  • Grasso M (1959) Fenome rigenerativi e apparato genitale in Dugesia lugubris. Boll Zool 26:523–527

    Google Scholar 

  • Hyman LH (1951) The invertebrates. II. Platyhelminthes and rhynchocoela, the acoelomate bilateria. McGraw-Hill, New York, p 118

    Google Scholar 

  • Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol (in press)

  • Morgan TH (1902) Growth and regeneration in Planaria lugubris. Arch Entwicklungsmech Org 13:179–212

    Article  Google Scholar 

  • Newmark and Alvarado (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142–153

    Article  PubMed  CAS  Google Scholar 

  • Ogawa K, Wakayama A, Kunisada T, Orii H, Watanabe K, Agata K (1998) Identification of a receptor tyrosine kinase involved in germ cell differentiation in planarians. Biochem Biophys Res Commun 248:204–209

    Article  PubMed  CAS  Google Scholar 

  • Orii H, Sakurai T, Watanabe K (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev Genes Evol 215:143–157

    Article  PubMed  CAS  Google Scholar 

  • Parisi M, Lin H (2000) Translational repression: a duet of nanos and pumilio. Curr Biol 10:R81–R83

    Article  PubMed  CAS  Google Scholar 

  • Sakai F, Agata K, Orii H, Watanabe K (2000) Organization and regeneration ability of spontaneous supernumerary eyes in planarians—eye regeneration field and pathway selection by optic nerves. Zool Sci 17:375–381

    Article  Google Scholar 

  • Saló E, Baguñà J (1985) Proximal and distal transformation during intercalary regeneration in the planarian Dugesia (S) mediterranea. Evidence using a chromosomal marker. Wilhelm Roux’s Arch Dev Biol 194:364–368

    Article  Google Scholar 

  • Saló E, Baguñà J (2002) Regeneration in planarians and other worms: new findings, new tools, and new perspectives. J Exp Zool 292(6):528–539

    Article  PubMed  Google Scholar 

  • Saló E, Pineda D, Marsal M, Gonzalez J, Gremigni V, Batistoni R (2002) Genetic network of the eye in platyhelminthes: expression and functional analysis of some players during planarian regeneration. Gene 287:67–74

    Article  PubMed  Google Scholar 

  • Saló E (2006) The power of regeneration and the stem-cell kingdom: freshwater planarians (platyhelminthes). BioEssays 28:546–559

    Article  PubMed  Google Scholar 

  • Salvetti A, Rossi L, Lena A, Batistoni R, Deri P, Rainaldi G, Locci M T, Evangelista M, Gremigni V (2005) DjPum, a homologue of Drosophila pumilio, is essential to planarian stem cell maintenance. Development 132(8):1863–74

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Shibata N, Orii H, Amikura R, Sakurai T, Agata K, Kobayashi S, Watanabe K (2006) Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Develop Growth Differ 48:615–628

    Article  CAS  Google Scholar 

  • Shibata N, Umesono Y, Orii H, Sakurai T, Watanabe K, Agata K (1999) Expression of vasa(vas)-related genes in germline cells and totipotent somatic stem cells of planarians. Dev Biol 206(1):73–87

    Article  PubMed  CAS  Google Scholar 

  • Torras R, Yanze N, Schmid V, González-Crespo S (2004) nanos expression at the embryonic posterior pole and the medusa phase in the hydrozoan Podocoryne carnea. Evol Dev 6 (5):362–371

    Article  PubMed  CAS  Google Scholar 

  • Tsuda M, Sasaoka Y, Kiso M, Abe K, Haraguchi S, Kobayashi S, Saga Y (2003) Conserved role of nanos proteins in germ cell development. Science 301:1239–1241

    Article  PubMed  CAS  Google Scholar 

  • Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209:31–39

    Article  PubMed  CAS  Google Scholar 

  • Zayas RM, Hernández A, Habermann B, Wang Y, Stary JM, Newmark PA (2005) The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 102 (51):18491–18496

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We would like to thank Dr. S González-Crespo for nanos primers, J González-Linares for initial PCRs with degenerate primers, Dr. H Orii for providing anti-VC-1, Dr. M Riutort for phylogenetic analysis, Dr. J Fernández and J Solana for advices on in situ hybridization on paraffin sections, Dr. R Romero and Dr. J Baguñà for discussions about planarian germ cells, Dr. F Cebrià for critical reading of the manuscript, and Dr. I. Patten for advice on English style in a version of the manuscript. This work was supported by grants BMC2002-03992 and BFU2005-00422 from the Ministerio de Educación y Ciencia, Spain, and grant 2005SGR00769 from AGAUR (Generalitat de Catalunya, Spain). M.H-T received an FPU fellowship from the Ministerio de Educación y Ciencia.

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Authors and Affiliations

  1. Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028, Barcelona, Spain

    Mette Handberg-Thorsager & Emili Saló

Authors
  1. Mette Handberg-Thorsager
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  2. Emili Saló
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Correspondence to Emili Saló.

Additional information

Communicated by V. Hartenstein

Electronic supplementary material

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S1

Nucleotide and deduced amino acid sequences of Smednos. The nucleotide sequence consists of four exons. The location of the three introns is indicated with black arrowheads and numbered from I-III. The cysteine and histidine residues of the conserved zinc-finger motifs are shown in bold and the two zinc-finger motifs are underlined in black. The start codon is underlined. The stop codon is indicated with an asterisk. The nucleotides and amino acids (in bold) are numbered in the right margin (DOC 59 kb)

S2

Alignment of amino acid sequence of the SmedNos zinc-finger motifs and flanking regions with representatives of the Nanos family using ClustalW. The cysteine and histidine residues of the zinc-finger motifs are underlined. The percentage identities are indicated on the right with SmedNos as the consensus sequence. Sequences used for the alignment indicating organism and accession number: Porifera (Ephydatia fluviatilis, PoNOS, BAB19253); Cnidaria (Hydra magnipapillata, CNNOS1, BAB01491; CNNOS2, BAB01492; Podocoryne carnea, PCNOS1, AAU11513; PCNOS2, AAU11514; Nematostella vectensis, NVNOS1, AAY67907; NVNOS2, AAY67908); Platyhelminthes (Schmidtea mediterranea, SmedNos, EF153633; Dugesia japonica, DjNOS, BAD88623.1); Arthropoda (Drosophila melanogaster, DmNos, AAA28715); Annelida (Helobdella robusta, Hro-Nos, AAB63111); Echinodermata (Hemicentrotus pulcherrimus, HpNanos, BAE53723); Chordata (Danio rerio, DanioNos, AAH97090; Xenopus laevis, Xcat-2, CAA51067; Mus musculus, MusNanos1, NP_848508; MusNanos2, NP_918953; MusNanos3, NP_918948; Homo sapiens, HsNanos1, Q8WY41; HsNanos2, P60321; HsNanos3, P60323) (DOC 109 kb)

S3

Phylogenetic tree obtained by Bayesian inference analysis of the amino acid sequences corresponding to the zinc-finger motifs and flanking regions of representatives of the Nanos family shown in S2. Branch lengths are proportional to numbers of substitutions per site indicated by the scale. Nanos from sponge, PoNOS, was used as the outgroup. SmedNos (highlighted in grey) forms a monophyletic group with Nanos from the protostomes, including Platyhelmintes (DjNOS), Arthropoda (DmNos) and Annelida (Hro-Nos). Accession numbers are indicated in S2 (DOC 69 kb)

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Handberg-Thorsager, M., Saló, E. The planarian nanos-like gene Smednos is expressed in germline and eye precursor cells during development and regeneration. Dev Genes Evol 217, 403–411 (2007). https://doi.org/10.1007/s00427-007-0146-3

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  • DOI: https://doi.org/10.1007/s00427-007-0146-3

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