Brefeldin A or monensin inhibits the 3D organizer in gastropod, polyplacophoran, and scaphopod molluscs

Gonzales, Eric E.; Zee, Maurijn van der; Dictus, Wim J.A.G.; Biggelaar, Jo Van Den

doi:10.1007/s00427-006-0118-z

Cited by 19 publications

(19 citation statements)

References 31 publications

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“…In spiral-cleaving embryos, this event is tied to the specification of the D quadrant during development [93]. In species where the first two embryonic cell divisions are unequal, the D quadrant is determined early by the asymmetric distribution of maternal cytoplasmic determinants, while in spiral-cleaving species that form equal-sized blastomeres at the 4-cell stage, the D quadrant is specified around the 24- to 32-cell stage by inductive interactions mediated by cell contacts between micromeres and macromeres [93–97]. In the current work, we found evidence that the specification of the D quadrant in the equal, biradial-cleaving bryozoan M. membranacea resembles that of equal, spiral-cleaving molluscs in the timing of specification, pattern of MAPK activation, and asynchrony of the D quadrant cell divisions post-specification.…”

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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“…In addition to the perturbed gastrulation, many Type 3 larvae resembled the exogastrulae that develop as a result of pharmacologically inhibiting the formation of the molluscan organizer (Damen and Dictus, '96;Nagy, 2001, 2003;Gonzales et al, 2007;Koop et al, 2007). In particular, the presence of multiple serotonergic cells in the pretrochal region is indicative of impairment of signaling derived from the 3D cell (Koop et al, 2007).…”

Section: Heat Shock Impacts On Morphogenesismentioning

confidence: 97%

Impact of ecologically relevant heat shocks on Hsp developmental function in the vetigastropod Haliotis asinina

Gunter

Degnan

2008

J Exp Zool Pt B

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Heat shock proteins (Hsps) are essential for cellular maintenance, normal differentiation and morphogenesis, and protection against a range of environmental stresses. It is unknown which of these roles takes precedence when they are required simultaneously. Here we examined the impact of thermal stress on the complex developmental expression patterns of HasHsp70 and HasHsp90A in the vetigastropod Haliotis asinina. We find that near-lethal heat shocks do not alter the spatial demarcation of Hsp expression despite such treatments impacting on the external character of the embryos. Using a suite of molecular markers that are both coexpressed with the Hsps (i.e. in ventrolateral ectoderm and prototroch) and expressed in tissues that have lower (basal) Hsp expression (e.g. serotonergic nervous system and shell gland), we determined that Hsp-expressing tissues do not incur markedly less thermal damage than adjacent tissues. To explore the relationship of Hsp expression with sensitivity of specific cell territories to heat shock, we focused on the formation of the prototroch, a tissue where HasHsp70 and HasHsp90A are coexpressed. By heat shocking at specific developmental stages, we determined that the most sensitive period of prototroch development is during its early specification and differentiation, which overlaps with the time the Hsps are expressed at their highest levels in these cells. This correlation is consistent with heat shock impairing the function of Hsps in regions of the H. asinina embryo undergoing morphogenesis.

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“…In spiral-cleaving embryos that have equal-sized blastomeres at the 4-cell stage, the future position of each quadrant is specified at a similar stage. In molluscs, for example, the interaction of the 3D macromere with the animal blastomeres at the 32-cell stage establishes the quadrant identities and the dorsoventral axis of the embryo (Biggelaar, 1977;Clement, 1962;Freeman and Lundelius, 1992;Gonzales et al, 2006;Martindale, 1986;Martindale et al, 1985). The MAPK pathway is the implicated molecular signaling underlying these events Koop et al, 2007;Lambert and Nagy, 2001;Lambert and Nagy, 2003).…”

Section: Onset Of Quadrant Identities and Mapk Activitymentioning

confidence: 99%

Cleavage modification did not alter early blastomere fates during bryozoan evolution

Vellutini

Martín-Durán

Hejnol

2016

Preprint

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Background: Spiral cleavage is a remarkably conserved pattern of embryogenesis present in animals of the clade Spiralia, such as annelids, molluscs, flatworms and nemerteans. However, not all spiralians display spiral cleavage. Recent phylogenies suggest that the spiral arrangement of embryonic blastomeres is an ancestral trait for the Spiralia and that it was secondarily modified in several spiralian lineages, such as gastrotrichs, brachiopods and bryozoans. To better understand the evolution of cleavage patterns in relation to blastomere fate maps and embryonic gene expression, we describe the cell lineage and molecular patterning in the embryogenesis of the bryozoan Membranipora membranacea.Results: M. membranacea develops through a unique stereotypic cleavage pattern with biradial symmetry and an embryo organized in identical quadrants with synchronous cell divisions. The quadrant identities are established as early as the 28-cell stage, when one vegetal blastomere (3D) activates the MAPK pathway, marking the future posterior region of the larva. Cells from this posterior quadrant divide asynchronously in subsequent stages leading to the morphological differentiation between quadrants. The first quartet of M. membranacea gives rise to the apical organ and ciliated band, the second and third quartet forms the oral/anal ectoderm, the fourth quartet the mesoderm and the vegetal blastomeres form the endoderm. We found that the early embryonic organization and the fate map of these early blastomeres in the bryozoan embryo are similar to a typical spiral-cleaving embryo. Furthermore we observe that correspondent blastomeres between the bryozoan and spiral-cleaving embryos share similar molecular identities, as revealed by the activity of MAPK and the expression of otx and foxa. The development of M. membranacea mainly differs from spiral-cleaving embryos in the downstream portions of the cell lineage, and in the origin of the mesoderm, which is formed by multiple fourth quartet blastomeres. Conclusions:The similarity between the fate map of M. membranacea and spiralcleaving embryos indicates that the cleavage geometry of the bryozoan evolved decoupled from other spiralian developmental traits. In this case, the blastomere fates remained evolutionarily conserved despite the drastic modification in the cleavage pattern from spiral to biradial. These findings suggest that blastomere fates of spiralcleaving embryos might not be linked to the stereotypic spiral cleavage pattern, but depend on other factors, such as the underlying molecular patterning. Our comparative analysis on the bryozoan reveals yet another facet of how early development evolves and helps to shed some light into the developmental diversity of spiralians. 2

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Brefeldin A or monensin inhibits the 3D organizer in gastropod, polyplacophoran, and scaphopod molluscs

Cited by 19 publications

References 31 publications

Cleavage modification did not alter blastomere fates during bryozoan evolution

Cleavage modification did not alter blastomere fates during bryozoan evolution

Impact of ecologically relevant heat shocks on Hsp developmental function in the vetigastropod Haliotis asinina

Cleavage modification did not alter early blastomere fates during bryozoan evolution

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