The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii

Steinmetz, Patrick R. H.; Kostyuchenko, R. P.; Fischer, Antje H. L.; Arendt, Detlev

doi:10.1111/j.1525-142x.2010.00457.x

Cited by 90 publications

(105 citation statements)

References 60 publications

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“…The expression of FoxA orthologs similarly anticipates blastopore formation in Hydroides and yolky Capitella embryos (Boyle and Seaver, 2008) despite their very distinct gastrulation by invagination and epiboly, respectively. In contrast, the early and broad endodermal expression of Brachyury and Otx is absent from the epibolic embryos of Platynereis (Steinmetz et al, 2011;Arendt et al, 2001), indicating that passive internalization of endoderm nephridium cells undergoing differentiation (Arenas-Mena, 2013).…”

Section: (1st Row) Gray and Colors Denote Vegetal Hemisphere Blastomentioning

confidence: 87%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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Hydroides elegans is an indirectly developing polychaete with equal spiral cleavage, gastrulation by invagination, and a feeding trochophore. Expression of several transcription factors and differentiation genes has been characterized. Comparative analysis reveals evolutionarily conserved roles. For example, the synexpression of transcription factors FoxA and Brachyury suggests homology of primary and secondary gut openings in protostomes and deuterostomes, and the expression of Sall suggests similar regulatory controls in the posterior growth zone of bilaterians. Differences in gene expression suggest regulatory differences control gastrulation by invagination in polychaetes with a feeding trochophore and gastrulation by epiboly in polychaetes without a feeding trochophore. Association of histone variant H2A.Z with transcriptional potency and its expression suggest a developmental role during both embryogenesis and the larva-to-adult transformation. Methods are being developed for experimental exploration of the gene regulatory networks involved in trochophore development in Hydroides. It is unknown if polychaete feeding trochophores evolved from a larval stage already present in the life cycle of the last common ancestor of protostomes and deuterostomes. Previous evolutionary scenarios about larval origins overemphasize the discontinuity between larval and adult development and require the early evolution of undifferentiated and transcriptionally potent "set aside" cells. Indirect development may proceed by developmental remodeling of differentiated cells and could have evolved after gradual transformation of juveniles into larvae; undifferentiated and transcriptionally potent cells would have evolved secondarily. Comprehensive characterization of gene regulatory networks for feeding trochophore development may help resolve these major evolutionary questions. KEY WORDS: bilaterian, posterior growth, serpulid, annelidHydroides elegans, a polychaete with a feeding trochophore Characterization of polychaetes with a feeding trochophore, such as Hydroides elegans ( Fig. 1 and Table 1), is relevant to understand the developmental evolution of complex life cycles in spiralians. Embryonic development in polychaetes conforms to the presence or absence of a feeding trochophore (Fig. 2). In the genus Hydroides (Eupomatus), embryogenesis ends in a feeding trochophore endowed with an equatorial ciliary band, a protonephridium, various sensory organs, and a functional gut formed after gastrulation by invagination (Hatschek, 1885;Shearer, 1911). Blastomeres 4d and 2d22 are inconspicuous and fated to contribute to the mesodermal and ectodermal portions of the segmented body that will have primarily a reproductive role; the Int. J. Dev. Biol. 58: 575-583 (2014) growth and proliferation of 4d and 2d22 are feeding-dependent. In contrast, during embryogenesis in polychaetes without feeding larvae, blastomeres 4d and 2d are relatively large and immediately engage in the formation of segments (Fig. 2). In addition to la...

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Section: (1st Row) Gray and Colors Denote Vegetal Hemisphere Blastomentioning

confidence: 87%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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“…Ectodermal spatial collinearity is absent in the two brachiopods even when the future location of the larval tissues after metamorphosis is considered (75,76). The anteriormost class gene lab is expressed exclusively in the chaetae of T. transversa and N. anomala, and thus is not affiliated with anterior neural or foregut tissues as in other lophotrochozoans, such as annelids (43,77). Similarly, the posteriormost Hox gene, Post1, is very transiently expressed in the chaetae sacs, which occupy a midposition in the larval body.…”

Section: Discussionmentioning

confidence: 99%

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Schiemann

Martín-Durán

Børve

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Temporal collinearity is often considered the main force preserving Hox gene clusters in animal genomes. Studies that combine genomic and gene expression data are scarce, however, particularly in invertebrates like the Lophotrochozoa. As a result, the temporal collinearity hypothesis is currently built on poorly supported foundations. Here we characterize the complement, cluster, and expression of Hox genes in two brachiopod species, Terebratalia transversa and Novocrania anomala. T. transversa has a split cluster with 10 genes (lab, pb, Hox3, Dfd, Scr, Lox5, Antp, Lox4, Post2, and Post1), whereas N. anomala has 9 genes (apparently missing Post1). Our in situ hybridization, real-time quantitative PCR, and stage-specific transcriptomic analyses show that brachiopod Hox genes are neither strictly temporally nor spatially collinear; only pb (in T. transversa), Hox3 (in both brachiopods), and Dfd (in both brachiopods) show staggered mesodermal expression. Thus, our findings support the idea that temporal collinearity might contribute to keeping Hox genes clustered. Remarkably, expression of the Hox genes in both brachiopod species demonstrates cooption of Hox genes in the chaetae and shell fields, two major lophotrochozoan morphological novelties. The shared and specific expression of Hox genes, together with Arx, Zic, and Notch pathway components in chaetae and shell fields in brachiopods, mollusks, and annelids provide molecular evidence supporting the conservation of the molecular basis for these lophotrochozoan hallmarks.chaetae | shell fields | Lophotrochozoa | Wiwaxia | Hox cluster

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“…6). These conditions resemble the morphology of P. dumerilii shortly before metamorphosis (Fischer et al, 2010, Steinmetz et al, 2011. In annelids, larvae usually exhibit a pair of single eyes consisting of one pigment cell and one photoreceptor cell, whereas most adults of Phyllodocida and Eunicida (including Nereididae) possess two pairs of so-called cerebral eyes (Purschke, 2005;Purschke et al, 2006).…”

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confidence: 99%

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

Helm¹,

Adamo²,

Hourdez³

et al. 2014

Int. J. Dev. Biol.

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The nereidid annelid Platynereis dumerilii emerged as a well-understood model organism. P. dumerilii and P. massiliensis are sister taxa, which are morphologically indistinguishable as adults. Interestingly, they exhibit highly contrasting life-histories: while P. dumerilii is a gonochorostic species with planktonic feeding larvae, P. massiliensis is a protandric hermaphrodite with lecitotrophic semi-direct -development in brood tubes. Using light microscopy and immunohistochemical methods coupled with confocal laser scanning microscopy, we describe the development of P. massiliensis. Musculature was stained with phalloidin-rhodamine. FMRFamide, acetylated a-tubulin, and serotonin were targeted by antibodies for the staining of neuronal structures. Additionally, eye development was investigated with the specific 22C10-antibody. The development of P. massiliensis is characterized by the absence of a free-swimming stage, a late development of food uptake, and the presence of a large amount of yolk even in late juvenile stages. Most notably, early juvenile stages already exhibit an organization of several organ systems that resembles those of adults. Larval characters present in the free-swimming feeding larvae of P. dumerilii, as e.g. the apical organ and larval eyes, are absent and regarded to be lost in developing stages of P. massiliensis. Many of the differences found in the development of these two species can be described in the context of heterochronic changes. We strongly advocate expanding evolutionary developmental studies from the well-established model annelid P. dumerilii to the closely related P. massiliensis to study the evolutionary conservation and divergence of genetic pathways involved in developmental processes. KEY WORDS: cLSM, evodevo, eye development, heterochrony, model organism, polychaeteThe vast majority of bilaterian animals are classified into three large clades: Deuterostomia, Ecdysozoa and Lophotrochozoa. Whereas several animal model systems for evolutionary developmental research are well established for the former two taxa, lophotrochozoans are underrepresented in this regard (GIGA Community of Scientists, 2014). However, especially in the last decade the annelid Platynereis dumerilii emerged as a well-understood model species (Fischer and Dorresteijn, 2004;Fischer et al., 2010;Simakov et al., 2013). Consequently, techniques as whole mount in situ hybridization, cell ablation, RNAinterference, and morpholino knockdowns are well established (Tessmar-Raible and Arendt, 2003;Veedin-Rajan et al., 2013). Moreover, transgenic lineages have been created (Backfisch et al., 2013) and a genome sequencing project is underway for this species (http://4dx.embl.de/platy/). Evolutionary developmental studies on Platynereis dumerilii provided important insights into the evolution of segmentation, vision and Int. J. Dev. Biol. 58: 613-622 (2014) doi: 10.1387/ijdb.140081cb the nervous system in Bilateria (Prud'homme et al., 2003;Arendt et al., 2004; Denes et al., 2007;Tessmar-Raible et al...

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The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii

Cited by 90 publications

References 60 publications

Development of a feeding trochophore in the polychaete Hydroides elegans

Development of a feeding trochophore in the polychaete Hydroides elegans

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

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