Mesoderm in spiralians: the organizer and the 4d cell

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...

Section: B C D E a Spiralian Gastrulation 415mentioning

confidence: 99%

Ins and outs of Spiralian gastrulation

Lyons¹,

Henry²

2014

Section: Observations On Sipunculan Developmentmentioning

confidence: 99%

“…The 4d cell divides to produce a pair of teloblasts that will form bands of mesoderm (Hatschek, 1883;Gerould, 1906), presumably homologous to endomesoderm in other spiralians where cell lineage/fate studies have been performed. A polar lobe has not been detected, and it is not known when or how the D quadrant is established or if there is a sipunculan organizer, although a combination of unequal cleavage and conspicuously large D macromere suggest the mechanism may be similar to what is implicated in mollusk and polychaete embryos (Clement, 1962;Henry and Martindale, 1999;Henry, 2002;Lambert, 2007Lambert, , 2010.No cell-lineage experiments by injection of intracellular tracers have been performed in a sipunculan embryo, and therefore direct cellfate characterizations in embryos or later stages are unavailable. Gastrulation in sipunculans occurs by epiboly with lecithotrophic development, and by invagination and/or epiboly in species with planktotrophic development (Hatschek, 1883;Åkesson, 1958;Rice, 1967;Rice, 1975b).…”

mentioning

confidence: 99%

“…Rice of the most basic and important problems have been worked out by decades of intensive studies on early determination of the Dquadrant, and precocious specification of the dorsal-ventral (D/V) axis, which are both associated with unequal cleavage (Freeman and Lundelius, 1992;Henry and Martindale, 1999). Therefore, future gene expression and bioinformatic experiments must also focus on the transcription factors and signaling pathways that are currently thought to regulate specification of the mesentoblast and the spiralian 'organizer' (Henry, 2002;Lambert, 2007), and other equally fundamental questions regarding sipunculan-specific cleavage asymmetries, and candidate genes that are likely to pattern some of their unique organ systems.The second major step will include an attempt to produce the very first embryonic fate map for a member of Sipuncula. As mentioned above, reproductive biology in T. lageniformis enables access to not only high numbers of eggs, but chemically controlled activation of eggs to obtain sequential batches of embryos.…”

mentioning

confidence: 99%

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Sipuncula: an emerging model of spiralian development and evolution

Boyle¹,

Rice²

2014

Sipuncula is an ancient clade of unsegmented marine worms that develop through a conserved pattern of unequal quartet spiral cleavage. They exhibit putative character modifications, including conspicuously large first-quartet micromeres and prototroch cells, postoral metatroch with exclusive locomotory function, paired retractor muscles and terminal organ system, and a U-shaped digestive architecture with left-right asymmetric development. Four developmental life history patterns are recognized, and they have evolved a unique metazoan larval type, the pelagosphera. When compared with other quartet spiral-cleaving models, sipunculan development is understudied, challenging and typically absent from evolutionary interpretations of spiralian larval and adult body plan diversity. If spiral cleavage is appropriately viewed as a flexible character complex, then understudied clades and characters should be investigated. We are pursuing sipunculan models for modern molecular, genetic and cellular research on evolution of spiralian development. Protocols for whole mount gene expression studies are established in four species. Molecular labeling and confocal imaging techniques are operative from embryogenesis through larval development. Nextgeneration sequencing of developmental transcriptomes has been completed for two species with highly contrasting life history patterns, Phascolion cryptum (direct development) and Nephasoma pellucidum (indirect planktotrophy). Looking forward, we will attempt intracellular lineage tracing and fate-mapping studies in a proposed model sipunculan, Themiste lageniformis. Importantly, with the unsegmented Sipuncula now repositioned within the segmented Annelida, sipunculan worms have become timely and appropriate models for investigating the potential for flexibility in spiralian development, including segmentation. We briefly review previous studies, and discuss new observations on the spiralian character complex within Sipuncula. KEY WORDS: pelagosphera, metatroch, unequal, U-shaped, ectomesoderm Ancient worms with a new statusSipuncula is a clade of unsegmented, coelomate marine worms. They have colonized benthic habitats worldwide from intertidal zones to abyssal plains in polar, temperate and tropical environments, and they have evolved a larval form that is unique among all metazoans, the pelagosphera (Mueller, 1850;Hatschek, 1883;Gerould, 1906;Rice, 1967). The adult body plan consists of a relatively large posterior trunk region with a single undivided coelomic cavity, and a retractable introvert with an array of tentacles on the anterior end that typically surrounds the mouth. The mouth leads to a U-shaped digestive system that terminates with an anus on the dorsal-anterior side of the trunk. Adult sipunculans have a centralized nervous system with a single, median, unsegmented Int. J. Dev. Biol. 58: 485-499 (2014) doi: 10.1387/ijdb.140095mb ventral nerve cord. There is comprehensive information on their reproductive biology (Rice, 1975b;Rice, 1989), anatomy (Rice, 1973(R...

“…The formation of the mesentoblast (i.e., 4d micromere) from the D quadrant, which is a conserved feature of spiralian development (Lambert, 2008;Lyons et al, 2012), is a consequence of D quadrant specification. In contrast, the particular micromeres that give rise to both mesoderm and ectoderm (i.e., ectomesoderm) vary among species.…”

Section: "That a Single Cell Can Carry The Total Heritage Of The Compmentioning

confidence: 99%

Developmental significance of D quadrant micromeres 2d and 4d in the oligochaete annelid Tubifex tubifex

Shimizu¹,

Nakamoto²

2014

The annelidTubifex tubifex is a cosmopolitan freshwater oligochaete and a member of the Spiralia, a large group of invertebrate phyla displaying spiral development. Because its developing eggs are easily obtained in the laboratory, this animal has long been used as material for developmental studies, especially spiralian embryology. In spiralian embryos, it has long been known that one blastomere at the four-cell stage, the D cell, and its direct descendants play an important role in axial pattern formation. Various studies have suggested that the D quadrant functions as the organizer of the embryonic axes in molluscs and annelids, and it has recently been demonstrated that the D quadrant micromeres, 2d 11 and 4d, which had been transplanted to an ectopic position in an otherwise intact embryo induce a secondary embryonic axis to give rise to the formation of duplicated heads and/or tails. That 2d and 4d play a pivotal role in Tubifex embryonic development was first suggested from the classic cell-ablation experiments carried out in the early 1920s, and this has been confirmed by the recent cell-ablation/restoration experiments using cell-labeling with lineage tracers. These studies have also shown that in the operated embryos, none of the remaining cells can replace the missing 2d and 4d and that both 2d and 4d are determined as ectodermal and mesodermal precursors, respectively, at the time of their birth. The anteroposterior polarity of these micromeres is also specified at the time of their birth, suggesting that nascent 2d and 4d are specified in their axial properties as well as in cell fate decision.