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Transcriptional control of unequal cleavage in early Tubifex embryos

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Abstract

Early embryos of the clitellate annelid Tubifex (oligochaete) undergo a series of unequal spiral cell divisions before the descendants of the D quadrant micromeres (cells 2d and 4d) divide bilaterally. Here, we show that inhibition of zygotic transcription by microinjection of α-amanitin (transcription inhibitor) exclusively converts unequal cleavage in cell 2d11 (granddaughter of 2d) into equal cleavage while other unequal cleavages and ensuing bilateral cleavages in cells 4d and 2d111 (great-granddaughter of 2d) all proceed in a normal fashion in the presence of this inhibitor. These results differ significantly from those reported for embryos of another clitellate annelid Helobdella (leech), in which inhibition of transcription converts bilateral (symmetric) cleavages in cells DNOPQ”’ and DM” (equivalent to 2d111 and 4d) into unequal (asymmetric) cleavages while having no apparent effect on unequal cleavage in DNOPQ” (equivalent to 2d11). These differences imply distinct mechanisms for the control of the unequal-to-bilateral transition in the two clitellate annelids.

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References

  • Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, Oxford

    Google Scholar 

  • Astrow SH, Holton B, Weisblat DA (1989) Teloplasm formation in a leech Helobdella triserialis is a microtubule-dependent process. Dev Biol 135:306–319

    Article  CAS  PubMed  Google Scholar 

  • Bergstralh DT, Dawney NS, St Johnston D (2017) Spindle orientation: a question of complex positioning. Development 144:1137–1145

    Article  CAS  PubMed  Google Scholar 

  • Bissen S, Smith CM (1996) Unequal cleavage in leech embryos: Zygotic transcription is required for correct spindle orientation in a subset of early blastomeres. Development 122:599–606

    CAS  PubMed  Google Scholar 

  • Bissen S, Weisblat DA (1991) Transcription in leech: mRNA synthesis is required for early cleavages in Helobdella embryos. Dev Biol 146:12–23

    Article  CAS  PubMed  Google Scholar 

  • Ishii R, Shimizu T (1995) Unequal first cleavage in the Tubifex egg: involvement of a monastral mitotic apparatus. Develop Growth Differ 37:687–701

    Article  Google Scholar 

  • Ishii R, Shimizu T (1997) Equalization of unequal first cleavage in the Tubifex egg by introduction of an additional centrosome: implications for the absence of cortical mechanisms for mitotic spindle asymmetry. Dev Biol 189:49–56

    Article  CAS  PubMed  Google Scholar 

  • Kitamura K, Shimizu T (2002) Segment-specific expression of alkaline phosphatase in the Tubifex embryo requires DNA replication and mRNA synthesis. J Exp Zool 294:68–76

    Article  CAS  PubMed  Google Scholar 

  • Lu MS, Johnston CA (2013) Molecular pathways regulating mitotic spindle orientation in animal cells. Development 140:1843–1856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyons DC, Weisblat DA (2009) D quadrant specification in the leech Helobdella: actomyosin contractility controls unequal cleavage of the CD blastomere. Dev Biol 334:46–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuo K, Yoshida H, Shimizu T (2005) Differential expression of caudal and dorsal genes in the teloblast lineages of the oligochaete annelid Tubifex tubifex. Dev Genes Evol 215:238–247

    Article  CAS  PubMed  Google Scholar 

  • Nakamoto A, Arai A, Shimizu T (2004) Specification of polarity of teloblastogenesis in the oligochaete annelid Tubifex: cellular basis for bilateral symmetry in the ectoderm. Dev Biol 272:248–261

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Shiomi I, Shimizu T (2017) Embryonic expression of festina lente (fel), a novel maternal gene, in the oligochaete annelid Tubifex tubifex. Gene Expr Patterns 25-26:29–35

    Article  CAS  PubMed  Google Scholar 

  • Penners A (1922) Die Furchung von Tubifex rivulorum Lam. Zool Jb Abt Anat Ontog 43:323–367

    Google Scholar 

  • Ren X, Weisblat DA (2006) Asymmetrization of first cleavage by transient disassembly of one spindle pole aster in the leech Helobdella robusta. Dev Biol 292:103–115

    Article  CAS  PubMed  Google Scholar 

  • Schmerer MW, Null RW, Shankland M (2013) Developmental transition to bilaterally symmetric cell divisions is regulated by Pax-mediated transcription in embryos of the leech Helobdella austinensis. Dev Biol 382:149–159

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T (1982a) Development in the freshwater oligochaete Tubifex. In: Harrison FW, Cowden RR (eds) Developmental biology of freshwater invertebrates. Alan R Liss, New York, pp 283–316

    Google Scholar 

  • Shimizu T (1982b) Ooplasmic segregation in the Tubifex egg: mode of pole plasm accumulation and possible involvement of microfilaments. Roux’s Arch Dev Biol 191:246–256

    Article  Google Scholar 

  • Shimizu T (1986) Bipolar segregation of mitochondria, actin network, and surface in the Tubifex egg: role of cortical polarity. Dev Biol 116:241–251

    Article  Google Scholar 

  • Shimizu T (1988) Localization of actin networks during early development of Tubifex embryos. Dev Biol 125:321–331

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T (1989) Asymmetric segregation and polarized redistribution of pole plasm during early cleavages in the Tubifex embryo: role of actin networks and mitotic apparatus. Develop Growth Differ 31:283–297

    Article  Google Scholar 

  • Shimizu T (1993) Cleavage asynchrony in the Tubifex embryo: involvement of cytoplasmic and nucleus-associated factors. Dev Biol 157:191–204

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T (1995a) Lineage-specific alteration in the cell cycle structure in early Tubifex embryos. Develop Growth Differ 37:263–272

    Article  Google Scholar 

  • Shimizu T (1995b) Role of the cytoskeleton in the generation of spatial patterns in Tubifex eggs. Cur Top Dev Biol 31:197–235

    Article  CAS  Google Scholar 

  • Shimizu T (1996) Behaviour of centrosomes in early Tubifex embryos: asymmetric segregation and mitotic cycle-dependent duplication. Roux’s Arch Dev Biol 205:290–299

    Article  Google Scholar 

  • Shimizu T, Nakamoto A (2001) Segmentation in annelids: cellular and molecular basis for metameric body plan. Zool Sci 18:285–298

    Article  Google Scholar 

  • Shimizu T, Ishii R, Takahashi H (1998) Unequal cleavage in the early Tubifex embryo. Develop Growth Differ 40:257–266

    Article  CAS  Google Scholar 

  • Shiomi I (2014) Experimental studies on the ontogeny of germ cells in the oligochaete annelid Tubifex tubifex. Master’s Thesis, Graduate School of Life Science, Hokkaido University, Sapporo.

  • Smith WC, Harland RM (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70:829–840

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Shimizu T (1997) Role of intercellular contacts in generating an asymmetric mitotic apparatus in the Tubifex embryo. Develop Growth Differ 39:351–362

    Article  CAS  Google Scholar 

  • Weisblat DA, Huang FZ (2001) An overview of glossiphoniid leech development. Can J Zool 79:218-232

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Acknowledgements

We thank members of the Shimizu laboratory for advice and help in collecting embryos. This study was supported in part by the Department of Biological Sciences.

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Authors and Affiliations

  1. Division of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo, 060-0810, Japan

    Momoe Aoki & Takashi Shimizu

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  1. Momoe Aoki
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  2. Takashi Shimizu
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Correspondence to Takashi Shimizu.

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Communicated by Mark Q. Martindale

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Aoki, M., Shimizu, T. Transcriptional control of unequal cleavage in early Tubifex embryos. Dev Genes Evol 227, 279–287 (2017). https://doi.org/10.1007/s00427-017-0584-5

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  • DOI: https://doi.org/10.1007/s00427-017-0584-5

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