Abstract
Segmentation is unquestionably a major factor in the evolution of complex body plans, but how this trait itself evolved is unknown. Approaching this problem requires comparing the molecular mechanisms of segmentation in diverse segmented and unsegmented taxa. Notch/Hes signaling is involved in segmentation in sequentially segmenting vertebrates and arthropods, as judged by patterns of expression of one or more genes in this network and by the disruption of segmental patterning when Notch/Hes signaling is disrupted. We have previously shown that Notch and Hes homologs are expressed in the posterior progress zone (PPZ), from which segments arise, in the leech Helobdella robusta, a sequentially segmenting lophotrochozoan (phylum Annelida). Here, we show that disrupting Notch/Hes signaling disrupts segmentation in this species as well. Thus, Notch/Hes functions in either the maintenance of the PPZ and/or the patterning processes of segmentation in representatives of all three superphyla of bilaterally symmetric animals. These results are consistent with two evolutionary scenarios. In one, segmentation was already present in the ancestor of all three superphyla. In the other, Notch/Hes signaling functioned in axial growth by terminal addition in an unsegmented bilaterian ancestor, and was subsequently exapted to function in segmentation as that process evolved independently in two or more taxa.
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References
Agee SJ, Lyons DC et al (2006) Maternal expression of a NANOS homolog is required for early development of the leech, Helobdella robusta. Dev Biol 298:1–11
Chipman AD, Akam M (2008) The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair-rule gene homologues. Dev Biol 319:160–169
Collins AG, Lipps JH et al (2000) Modern mucociliary creeping trails and the bodyplans of Neoproterozoic trace-makers. Paleobiology 26:47–55
Davis GK, Patel NH (1999) The origin and evolution of segmentation. Trends Biochem Sci 24:M68–M72
Geling A, Steiner H et al (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. Embo Rep 3:688–694
Gimlich RL, Braun J (1985) Improved fluorescent compounds for tracing cell lineage. Dev Biol 109:509–514
Kasbauer T, Towb P et al (2007) The Notch signaling pathway in the cnidarian Hydra. Dev Biol 303:376–390
Lewis J (2003) Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr Biol 13:1398–1408
Micchelli CA, Esler WP et al (2002) Gamma-secretase/presenilin inhibitors for Alzheimer’s disease phenocopy Notch mutations in Drosophila. Faseb J 16:79–81
Palmerim I, Henrique D et al (1997) Avian hairy gene expression identifies a molecular clock linked to vertebrate segmentation and somitogenesis. Cell 91:639–648
Rivera AS, Gonsalves FC et al (2005) Characterization of Notch-class gene expression in segmentation stem cells and segment founder cells in Helobdella robusta (Lophotrochozoa; Annelida; Clitellata; Hirudinida; Glossiphoniidae). Evol Dev 7:588–599
Shain DH, Ramirez-Weber FA et al (1998) Gangliogenesis in leech: morphogenetic processes leading to segmentation in the central nervous system. Dev Genes Evol 208:28–36
Shain DH, Stuart DK et al (2000) Segmentation of the central nervous system in leech. Development 127:735–744
Shankland M, Savage RM (1997) Annelids, the segmented worms. In: Gilbert SF, Raunio AM (eds) Embryology: constructing the organism. Sinauer, Sunderland, pp 219–235
Song MH (2000) Characterization of hairy/E(spl)- and eve-class genes in the posterior growth zone of the leech Helobdella robusta, a segmented lophotrochozoan. Biophysics. Berkeley, University of California, Berkeley, p 179
Song MH, Huang FZ et al (2002) Expression and function of an even-skipped homolog in the leech Helobdella robusta. Development 129:3681–3692
Song MH, Huang FZ et al (2004) Cell cycle-dependent expression of a hairy and Enhancer of split (hes) homolog during cleavage and segmentation in leech embryos. Dev Biol 269:183–195
Stollewerk A, Schoppmeier M et al (2003) Involvement of Notch and Delta genes in spider segmentation. Nature 423:863–865
Weisblat DA, Shankland M (1985) Cell lineage and segmentation in the leech. Philos T Roy Soc B 312:39–56
Woodruff J, Mitchell B et al (2007) Hau-Pax3/7A is an early marker of leech mesoderm involved in segmental morphogenesis, nephridial development, and body cavity formation. Dev Biol 306:824–837
Zackson SL (1984) Cell lineage, cell cell-interaction, and segment formation in the ectoderm of a glossiphoniid leech embryo. Dev Biol 104:143–160
Acknowledgements
This work was supported by NIH RO1 GM 60240 to DAW. We thank members of our lab for many helpful discussions and comments on this manuscript.
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Communicated by M. Martindale
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Rivera, A.S., Weisblat, D.A. And Lophotrochozoa makes three: Notch/Hes signaling in annelid segmentation. Dev Genes Evol 219, 37–43 (2009). https://doi.org/10.1007/s00427-008-0264-6
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DOI: https://doi.org/10.1007/s00427-008-0264-6