Molecular Basis of Annelid Segmentation

In contrast to the relatively good understanding of the main molecular players during the segmentation process of arthropods and vertebrates, mechanistic knowledge of the gene networks controlling segment development in annelids is very scant. The main reason for this lag, besides the fact that developmental biology of annelids is a much less populated field than that of arthropods or vertebrates, is the historical lack of strong functional molecular tools applicable to annelid models. More recently, however, the emergence of transcriptional profiling approaches, combined with powerful and broadly applicable gene editing techniques (e.g., Crispr-CAS9 gene editing) are lifting this constraint, and many research programs are currently working on providing better answers to the question of how annelids organize their tissues into segmental units.

Most approaches to uncovering the molecular genetic basis of segment formation in annelids have revolved around candidate gene approaches (see Bleidorn et al., 2015, for a summary): orthologs of genes known to be involved in the arthropod segmentation process (especially those known from Drosophila fruit flies) were identified in several annelid species, and their expression patterns during development were explored using in situ mRNA hybridization assays. Initial results were interpreted as supporting the existence of segmentation mechanisms common to both arthropods and annelids, or even to vertebrates. Then, when evidence from molecular phylogenies led to rejection of the Articulata hypothesis that Arthropoda and Annelida are closely related, these same data were interpreted as supporting the hypothesis of a truly segmented last common ancestor of all bilaterians.

However, closer examination of the data concerning segmentation gene homologs has raised doubts about this interpretation. In some cases, the spatial and temporal patterns of expression proved incompatible with the putative roles of the genes in segmentation. In other cases, it was realized that the candidate genes are broadly expressed during various aspects of development in diverse taxa, thus weakening the argument that similar patterns are indicative of shared ancestry—any gene involved in building any component of a segment will show an iterated, segmental pattern. For example, the genes wntl/wingless and engrailed (en) interact in Drosophila to define para-segmental boundaries (Heuvel et al. 1993). Initial studies of expression of these genes in Platynereis showed a pattern consistent with a role in defining segment polarity in this species (Prud’homme et al. 2003): Pdu-en is expressed at the anterior portion of developing segments, while Pdu-wntl is expressed in their posterior part. These findings were hailed as evidence of a common arthropod-annelid patterning system. However, investigations in other groups failed to support the generality of the Platynereis pattern: expression of en in Chaetopterus, Capitella, and Hydroides is not compatible with a fundamental early role in segmentation (Seaver et al. 2001; Seaver and Kaneshige 2006). In addition, experiments in the leech Helobdella show that ablation of си-expressing cells within clones of ectoteloblast progeny does not affect establishment of segment polarity (Seaver and Shankland 2001). Similar disagreements have been found for other fly segmentation genes, like hedgehog (Seaver and Kaneshige 2006; Kang et al. 2003; Dray et al. 2010), even-skipped {eve), runt, and paired (prd, Pax3/7 Song et al. 2002; de Rosa, Prud’homme, and Balavoine 2005; Seaver et al. 2012) and hunchback (Iwasa, Suver, and Savage 2000; Werbrock et al. 2001; Kerner et al. 2006). In most cases, a candidate gene found expressed in developing segments was found to also show broad expression at other places and times, suggesting that even if they do play a role in segmentation, then convergent co-option of a widely used toolkit gene is a more parsimonious hypothesis than developmental homology inherited from the last common ancestor between arthropods and annelids or a segmented last common bilaterian ancestor.

Perhaps a notable exception to the aforementioned disagreements is the Notch and hairy (hes) genes known to be involved in arthropod and vertebrate segmentation. In Platynereis, Notch expression has not been described, but 15 paralogues of hairy have been reported, 7 of which show expression patterns consistent with a role in segmentation (Gazave, Guillou, and Balavoine 2014). Six of them (Pdu-Hesl/2, 4, 5, 6, and 8) are expressed in the ectoteloblast ring around the posterior growth zone (PGZ). Pdu-Hes5 is also expressed in the underlying ring of mesoteloblasts derived from 4d descendants (see earlier). In all cases, Hes expression is associated with the established PGZ but not with earlier development of the mesoteloblast lineage. In Capitella, the patterns of Notch and hes expression during embryonic development do not support the hypothesis that these genes play an interacting role in segmentation; however, Capl-hesl shows transient expression in small bands of pre-segmental mesoderm in larvae, and later in small mesodermal domains of the PGZ of late larvae and juveniles (Thamm and Seaver 2008). In contrast, in juveniles and adults, Capl-Delta, Capl-Notch, Capl-hesl, Capl-hes2, and Capl-hes3 are all expressed in the PGZ, even though their expression doesn’t extend anteriorly to developing segments. Interestingly, while Cap-hesl expression is limited to unsegmented mesoderm, its anterior boundary is the posterior boundary of the nascent segment, which is also the posterior limit of Capl-Delta and Capl-Notch expression domains. Capl-hes2 and Capl-hes3 expression straddles this boundary and extends both anteriorly into the forming segment and posteriorly into the unsegmented segment addition zone. One interpretation of these data is that segmentation at the PGZ involves progenitor stem cells that maintain Capl-hesl expression independently of Capl-Notch, which instead has a role in segment boundary formation (Thamm and Seaver 2008). Involvement of Notch and hes has also been shown in leeches, where experimental simultaneous disruption of Notch signaling and hes expression results in somewhat weak segmentation defects of ectoteloblast progeny (Rivera and Weisblat 2009). Such treatment did not affect teloblast division and blast cell formation, the primary mechanism behind lineage-driven segmentation, nor did it interfere with clonal expansion, but the clones failed to generate regular and seg- mentally iterated patterns. Evidence of the generalized involvement of Notch and hes in annelid segmentation suggests this mechanism is part of the annelid ground plan and supports its presence in the last common ancestors of this phylum, arthropods and vertebrates. However, this does not imply a segmented Urbilateria: Notch/ hes signaling might also have been involved in posterior elongation and co-opted independently during the evolution of segmentation in each phylum (Chipman 2010).

Thus, our knowledge about the molecular underpinnings of annelid segmentation is still too limited to make any broad statement about conservation or variability of genes, gene regulatory networks, or developmental processes across the segmented phyla. But there is hope that recent developments on functional molecular research tools will soon begin to shed new light on how different annelid groups organize their cells and tissues into repeated metameric units.

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