Segmentation in Annelids: Cellular and Molecular Basis for Metameric Body Plan

Shimizu, Takashi; Nakamoto, Ayaki

doi:10.2108/zsj.18.285

Cited by 31 publications

(26 citation statements)

References 65 publications

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“…Goulding [20,80] used a modified naming system based on Conklin’s nomenclature that applied the prefix 4d and superscripts for left/right 4d R /4d L (equal to ML and MR), which were then followed by numbers to denote the further divisions, with 1 being applied to the more animal daughter and 2 applied to the more vegetal daughter. A specific nomenclature exists for 4d sublineages in clitellate annelids, which develop via a modified spiral cleavage program that gives rise to exceptionally large ectodermal and mesodermal stem cells called teloblasts [9,17,62,81,82]. For example, in the leech Helobdella the homolog of 4d, DM" divides bilaterally giving rise to two mesodermal stem cells, the M L and M R teloblasts.…”

Section: Discussionmentioning

confidence: 99%

Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Lyons

Perry

Lesoway

et al. 2012

EvoDevo

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BackgroundAnimals with a spiral cleavage program, such as mollusks and annelids, make up the majority of the superphylum Lophotrochozoa. The great diversity of larval and adult body plans in this group emerges from this highly conserved developmental program. The 4d micromere is one of the most conserved aspects of spiralian development. Unlike the preceding pattern of spiral divisions, cleavages within the 4d teloblastic sublineages are bilateral, representing a critical transition towards constructing the bilaterian body plan. These cells give rise to the visceral mesoderm in virtually all spiralians examined and in many species they also contribute to the endodermal intestine. Hence, the 4d lineage is an ideal one for studying the evolution and diversification of the bipotential endomesodermal germ layer in protostomes at the level of individual cells. Little is known of how division patterns are controlled or how mesodermal and endodermal sublineages diverge in spiralians. Detailed modern fate maps for 4d exist in only a few species of clitellate annelids, specifically in glossiphoniid leeches and the sludge worm Tubifex. We investigated the 4d lineage in the gastropod Crepidula fornicata, an established model system for spiralian biology, and in a closely related direct-developing species, C. convexa.ResultsHigh-resolution cell lineage tracing techniques were used to study the 4d lineage of C. fornicata and C. convexa. We present a new nomenclature to name the progeny of 4d, and report the fate map for the sublineages up through the birth of the first five pairs of teloblast daughter cells (when 28 cells are present in the 4d sublineage), and describe each clone’s behavior during gastrulation and later stages as these undergo differentiation. We identify the precise origin of the intestine, two cells of the larval kidney complex, the larval retractor muscles and the presumptive germ cells, among others. Other tissues that arise later in the 4d lineage include the adult heart, internal foot tissues, and additional muscle and mesenchymal cells derived from later-born progeny of the left and right teloblasts. To test whether other cells can compensate for the loss of these tissues (that is, undergo regulation), specific cells were ablated in C. fornicata.ConclusionsOur results present the first fate map of the 4d micromere sublineages in a mollusk. The fate map reveals that endodermal and mesodermal fates segregate much later than previously thought. We observed little evidence of regulation between sublineages, consistent with a lineage-driven cell specification process. Our results provide a framework for comparisons with other spiralians and lay the groundwork for investigation of the molecular mechanisms of endomesoderm formation, germ line segregation and bilateral differentiation in Crepidula.

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Section: Discussionmentioning

confidence: 99%

Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Lyons

Perry

Lesoway

et al. 2012

EvoDevo

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“…Furthermore the paraphyly of the polychaetes has implications for the origin of the clitellates. Again segmentation is an issue, with different modes apparently operating in polychaetes versus clitellates (Shimizu & Nakamoto, 2001;Irvine & Seaver, 2006). Also the annelid ancestor clearly underwent indirect development via a trochophore larva ( Fig.…”

Section: The Annelid Ancestormentioning

confidence: 99%

“…2D) 1999), a reproductive process has evolved which involves the clitellum and the formation of a cocoon in which the embryos are nourished on a supply of yolk and have done away with the requirement for a feeding trochophore larva. Further to this, development via large teloblast cells is employed by the leech and oligochaetes (Weisblat & Huang, 2001;Bergter et al, 2004), and the evolutionary relationship between these leech teloblasts and cells in the posterior growth zone of polychaetes is an important issue to be resolved (de Rosa et al, 2005;Shimizu & Nakamoto, 2001;Seaver et al, 2005). The discussions on the reconstruction of the annelid and clitellate ancestors have been reviewed in greater detail elsewhere (e.g.…”

Section: The Annelid Ancestormentioning

confidence: 99%

Annelids in evolutionary developmental biology and comparative genomics

et al. 2008

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Summary :Annelids have had a long history in comparative embryology and morphology, which has helped to establish them in zoology textbooks as an ideal system to understand the evolution of the typical triploblastic, coelomate, protostome condition. In recent years there has been a relative upsurge in embryological data, particularly with regard to the expression and function of developmental control genes. Polychaetes, as well as other annelids such as the parasitic leech, are now also entering the age of comparative genomics. All of this comparative data has had an important impact on our views of the ancestral conditions at various levels of the animal phylogeny, including the bilaterian ancestor and the nature of the annelid ancestor. Here we review some of the recent advances made in annelid comparative development and genomics, revealing a hitherto unsuspected level of complexity in these ancestors. It is also apparent that the transition to a parasitic lifestyle leads to, or requires, extensive modifications and derivations at both the genomic and embryological levels.

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“…Le blastomère 2d a une destinée ectodermique, le second est l'initiale mésodermique. Leur devenir, bien connu sous ses aspects descriptifs chez la Néreis, associé au développement de la larve trocophore, a été analysé de façon fine, jusqu'au plan génétique, chez les clitellates, dont le développement est direct, les hirudinées (achètes) Helobdella stagnalis, Theromyzon rude et tessulatum [17] et l'oligochète Tubifex [18], notamment. Audelà de différences dans les modalités de la gastrulation entre les polychètes et les clitellates, les mouvements et les divisions de ces blastomères conduisent, dans les deux cas, à la mise en place de cellules de grande taille, les téloblastes.…”

Section: Annélides Et Arthropodesunclassified

“…Le maintien des limites segmentaires repose sur des interactions réciproques entre cellules adjacentes via les messagers à rayon d'action local que sont la protéine hedgehog, sécrétée par les cellules exprimant engrailed, et la protéine wingless (Figure 2). Les homologues de hedgehog ont été isolés et leur expression étudiée chez l'hirudiné Helobdella robusta [28], les insectes Schistocerca [18] et Gryllus bimaculatus [29], le myriapode Glomeris marginata [30], le crustacé Artemia salina, le chélicérate Euscorpius flavicaudis [11], les procordés Amphioxus [31] et Ciona [32], ainsi que chez les vertébrés. L'expression précoce, dans beaucoup de cas, a pu être associée à la segmentation, comme elle l'est chez la drosophile.…”

Section: Segmentation Du Corps : Aspects Moléculaires Et Génétiquesunclassified

Urbilateria, un être évolué ?

Cornec

Gilles

2006

Med Sci (Paris)

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Segmentation in Annelids: Cellular and Molecular Basis for Metameric Body Plan

Cited by 31 publications

References 65 publications

Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

Annelids in evolutionary developmental biology and comparative genomics

Urbilateria, un être évolué ?

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