Embryonic origins of hull cells in the flatworm Macrostomum lignano through cell lineage analysis: developmental and phylogenetic implications

Willems, Maxime; Egger, Bernhard; Wolff, Carsten; Mouton, Stijn; Houthoofd, Wouter; Fonderie, Pamela; Couvreur, Marjolein; Artois, Tom; Borgonie, Gaëtan

doi:10.1007/s00427-009-0304-x

Cited by 13 publications

(15 citation statements)

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“…In most of these cases, the embryonic development has changed to such extent that no traces of spiral cleavage are found, and the ancestral cleavage geometry can only be inferred by the phylogenetic position of the clade (e.g., the discoidal cleavage of cephalopods [25]). Remnants of spiral cleavage usually consist of oblique mitotic spindles, as in the flatworm Macrostomum lignano , which displays a typical spiral cleavage pattern until the third cleavage, when the embryonic development becomes considerably modified [159]. The bryozoan M. membranacea differs from these previously known cases because we can recognize shared cell lineage and developmental traits with spiral-cleaving embryos that are not the cleavage geometry itself.…”

Section: Discussionmentioning

confidence: 99%

Cleavage modification did not alter blastomere fates during bryozoan evolution

2017

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BackgroundStereotypic cleavage patterns play a crucial role in cell fate determination by precisely positioning early embryonic blastomeres. Although misplaced cell divisions can alter blastomere fates and cause embryonic defects, cleavage patterns have been modified several times during animal evolution. However, it remains unclear how evolutionary changes in cleavage impact the specification of blastomere fates. Here, we analyze the transition from spiral cleavage – a stereotypic pattern remarkably conserved in many protostomes – to a biradial cleavage pattern, which occurred during the evolution of bryozoans.ResultsUsing 3D-live imaging time-lapse microscopy (4D-microscopy), we characterize the cell lineage, MAPK signaling, and the expression of 16 developmental genes in the bryozoan Membranipora membranacea. We found that the molecular identity and the fates of early bryozoan blastomeres are similar to the putative homologous blastomeres in spiral-cleaving embryos.ConclusionsOur work suggests that bryozoans have retained traits of spiral development, such as the early embryonic fate map, despite the evolution of a novel cleavage geometry. These findings provide additional support that stereotypic cleavage patterns can be modified during evolution without major changes to the molecular identity and fate of embryonic blastomeres.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0371-9) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Cleavage modification did not alter blastomere fates during bryozoan evolution

2017

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“…For example, ectolecithal development is common, in which yolk is extraembryonic, and must be incorporated into cells later in development (Martín-Durán and Egger, 2012). In some platyhelminth species, vegetally-derived "hull" cells envelop the embryo primordium by a process of reverse epiboly (Willems et al, 2009). Some species exhibit what is called anarchic cleavage, where individual blastomeres migrate through the yolk in the egg capsule, and in these cases, development is so modified that some authors have argued that no comparisons to gastrulation in other embryos can be made (discussed by Martín-Durán and Egger, 2012).…”

Section: Intermediate Forms Emboly and Other Variations On Gastrulationmentioning

confidence: 99%

Ins and outs of Spiralian gastrulation

Lyons¹,

Henry²

2014

Int. J. Dev. Biol.

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Gastrulation is a critical stage of metazoan development during which endodermal and mesodermal tissues are internalized, and morphogenesis transforms the early embryo into each animal's unique body-plan. While gastrulation has been studied extensively in classic model systems such as flies, worms, and vertebrates, less is known about gastrulation at a mechanistic level in other taxa. Surprisingly, one particularly neglected group constitutes a major branch of animals: the Spiralia. A unique feature of spiralian development is that taxa with diverse adult body-plans, such as annelids, molluscs, nemerteans and platyhelminths all share a highly stereotyped suite of characters during embryogenesis called spiral cleavage. The spiral cleavage program makes it possible to compare distantly related embryos using not only morphological features, and gene expression patterns, but also homologous cell lineages. Having all three criteria available for comparison is especially critical for understanding the evolution of a complex process like gastrulation. Thus studying gastrulation in spiralians is likely to lead to novel insights about the evolution of body-plans, and the evolution of morphogenesis itself. Here we review relevant literature about gastrulation in spiralians and frame questions for future studies. We describe the internalization of the endoderm, endomesoderm and ectomesoderm; where known, we review data on the cellular and molecular control of those processes. We also discuss several morphogenetic events that are tied to gastrulation including: axial elongation, origins of the mouth and anus, and the fate of the blastopore. Since spiral cleavage is ancestral for a major branch of bilaterians, understanding gastrulation in spiralians will contribute more broadly to ongoing debates about animal body-plan divergence, such as: the origin of the through-gut, the emergence of indirect versus direct development, and the evolution of gene-regulatory networks that specify endomesoderm. We emphasize the fact that spiralian gastrulation provides the unique opportunity to connect well-defined embryonic cell lineages to variation in cell fate and cell behavior, making it an exceptional case study for evo-devo. KEY WORDS: spiralia, endomesoderm, ectomesoderm, blastopore, axial elongation, epiboly, invagination Gastrulation is a critical embryonic event during which presumptive endodermal and mesodermal cells are internalized (Stern, 2004). Gastrulation is closely tied to the development of key axial properties, and to the patterning of certain organ systems, such as the digestive tract; the openings of the mouth and/or anus often arise at or close to the site of gastrulation, called the blastopore (see Technau and Scholz, 2003;Hejnol and Martindale, 2009). Gastrulation also holds a pivotal role in evolutionary theories about the emergence and divergence of bilaterian body-plans (Arendt and Nübler-Jung,1997;Nielsen, 2001;Martindale and Hejnol, 2009 As evo-devo questions go, tracing the evolutionary history o...

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“…Three polar bodies are extruded at the animal pole, which later become incorporated into the embryo ( Macrostomum appendiculatum, M. lignano ). Large cytoplasmatic protuberances ("blebbing") occur predominantly in the undivided oocyte, but are also seen during cleavage [35,37,38]. At the two-cell stage, one blastomere (CD) is usually slightly larger than the other (AB), and by laeotropic (left-handed) division arrives at the four-cell-stage, where blastomere D is often, but not always largest.…”

Section: Reviewmentioning

confidence: 99%

Developmental diversity in free-living flatworms

Martín-Durán

Egger

2012

EvoDevo

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Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes (excluding Acoelomorpha) are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms. Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis. Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms. While some more basally branching groups - such as polyclad flatworms - retain the ancestral quartet spiral cleavage pattern, most flatworms have significantly diverged from this pattern and exhibit unique strategies to specify the common adult body plan. Most free-living flatworms (i.e. Platyhelminthes excluding the parasitic Neodermata) are directly developing, whereas in polyclads, also indirect developers with an intermediate free-living larval stage and subsequent metamorphosis are found. A comparative study of developmental diversity may help understanding major questions in evolutionary biology, such as the evolution of cleavage patterns, gastrulation and axial specification, the evolution of larval types, and the diversification and specialization of organ systems. In this review, we present a thorough overview of the embryonic development of the different groups of free-living (turbellarian) platyhelminths, including the Catenulida, Macrostomorpha, Polycladida, Lecithoepitheliata, Proseriata, Bothrioplanida, Rhabdocoela, Fecampiida, Prolecithophora and Tricladida, and discuss their main features under a consensus phylogeny of the phylum.

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Embryonic origins of hull cells in the flatworm Macrostomum lignano through cell lineage analysis: developmental and phylogenetic implications

Cited by 13 publications

References 58 publications

Cleavage modification did not alter blastomere fates during bryozoan evolution

Cleavage modification did not alter blastomere fates during bryozoan evolution

Ins and outs of Spiralian gastrulation

Developmental diversity in free-living flatworms

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