Cleavage modification did not alter blastomere fates during bryozoan evolution

Abstract

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.

Expression of six3 and otx in Solenogastres (Mollusca) supports an ancestral role in bilaterian anterior‐posterior axis patterning

“…However, additional expression in the ciliary bands or the shell gland, as described from a gastropod veliger (Perry et al, 2015), seems to be lacking in aculiferan mollusks. The apical expression pattern is also in accordance with the pattern described in ciliated larvae of other lophotrochozoans (Hiebert & Maslakova, 2015ab;Marlow et al, 2014;Santagata et al, 2012;Steinmetz et al, 2010;Vellutini et al, 2017), as well as deuterostomes (Poustka et al, 2007;Wei et al, 2009) and cnidarians (Marlow et al, 2013;Sinigaglia et al, 2013), where it is also mainly expressed in the area around the apical organ but never in the apical tuft cells proper. As in gastropods, additional six3 expression in the ciliary bands is present in nemertine pilidium and sea urchin pluteus larvae (Hiebert & Maslakova, 2015b;Wei et al, 2009).…”

“…Prototrochal expression of otx is widespread among annelid larvae (Arenas-Mena & Wong, 2007;Arendt et al, 2001;Steinmetz et al, 2007Steinmetz et al, , 2011 for an exception, see the polychaete Capitella telata, Boyle et al, 2014). It may thus have been present in the LCA of mollusks and annelids, but the expression of otx in the ciliary band of a bryozoan larva (Vellutini et al, 2017) could hint to an even earlier evolutionary emergence of this character within the lophotrochozoans.…”

“…In planktonic ciliated larvae of cnidarians, protostomes, and deuterostomes, s ix3 is expressed anteriorly in the area around the major sensory structure of these larvae, the apical organ, but never in the cells that bear the cilia of the apical tuft (Hiebert & Maslakova, 2015ab; Marlow, Matus, & Martindale, ; Marlow et al, ; Poustka et al, ; Perry et al, ; Steinmetz et al, ; Santagata, Resh, Hejnol, Martindale, & Passamaneck, ; Sinigaglia, Busengdal, Leclère, Technau, & Rentzsch, ; Vöcking, Kourtesis, & Hausen, ; Vellutini, Martín‐Durán, & Hejnol, ; Wei, Yaguchi, Yaguchi, Angerer, & Angerer, ). Only in Platynereis dumerilii , expression in a low number of other cells belonging to the apical organ has been demonstrated (Marlow et al, ).…”

“…Otx is expressed more abapically than six3 , in the region of the ciliary bands in both protostome and deuterostome planktonic larvae (Arenas‐Mena & Wong, ; Arendt, Technau, & Wittbrodt, ; Gan et al, ; Harada et al, ; Hinman, Nguyen, & Davidson, ; Lowe & Wray, ; Lowe, Issel‐Tarver, & Wray, ; Nederbragt, te Welscher, van den Driesche, van Loon, & Dictus, ; Perry et al, ; Shoguchi, Harada, Numakunai, & Satoh, ; Steinmetz, Zelada‐Gonzáles, Burgtorf, Wittbrodt, & Arendt, ; Steinmetz et al, , ; Vöcking et al, ; Vellutini et al, ). Additionally, otx expression is present in parts of the posttrochal ectoderm and in the gut in larvae of annelids, gastropods, and echinoids (Arenas‐Mena & Wong, ; Boyle, Yamaguchi, & Seaver, ; Gan et al, ; Nederbragt et al, ; Perry et al, ) as well as in the CNS of annelid and gastropod larvae (Arendt et al, ; Boyle et al, ; Perry et al, ; Vöcking et al, ).…”

BioCell2XML: A novel tool for converting cell lineage data from SIMI BioCell to MaMuT (Fiji)

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Computer-assisted 4D manual cell tracking has been a valuable method for understanding spatial-temporal dynamics of embryogenesis (e.g., Stach & Anselmi, 2015;Vellutini et al, 2017;Wolff et al, 2018) since the method was introduced in the late 1990s. Since two decades SIMI® BioCell (Schnabel et al, 1997), a software which initially was developed for analyzing data coming from the, at that time new technique of 4D microscopy, is in use.Many laboratories around the world use SIMI BioCell for the manual tracing of cells in embryonic development of various species to reconstruct cell genealogies with high precision.However, the software has several disadvantages: Limits in handling very large data sets, the virtually no maintenance over the last ten years (bound to older Windows versions), the difficulty to access the created cell lineage data for analyses outside SIMI BioCell, and the high cost of the program.

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