The transcription factors HeBlimp and HeT‐brain of an indirectly developing polychaete suggest ancestral endodermal, gastrulation, and sensory cell‐type specification roles

Abstract

The expression of Blimp and T-brain was characterized during embryogenesis of the indirectly developing polychaete Hydroides elegans. The expression of both genes in the vegetal blastomeres of this lophotrochozoan is restricted to the lateral and oral regions of the blastopore. Both transcription factors also have expression patterns consistent with ancestral neural functions. HeBlimp is expressed in a couple of animal cap cells and exhibits a marked left bias that correlates with earlier development of the left eye in H. elegans. HeT-brain is expressed in animal cap blastomeres and eventually becomes restricted to apical tuft cells of early trochophore stages. The expression of Blimp and T-brain among directly and indirectly developing bilaterians suggests ancestral sensory cell-type specification, gastrulation by invagination, endoderm specification, mesoderm specification, and/or tripartite gut subdivision. These characterizations add to the long-term goal of understanding the regulatory evolution functions that underlies complex life cycles in metazoans.

Development of a feeding trochophore in the polychaete Hydroides elegans

“…Despite their respective sinistral and dextral patterns, in Hydroides elegans and Hydroides eupomatus the operculum develops first on the left side, suggesting that left-right asymmetries in the genus are independent of spiralcleavage chirality. Asymmetry in the order of eye formation has been described among serpulid species (Segrove, 1941;Wisely, 1958;Arenas-Mena, 2008), but its correlation with cleavage chirality remains uncertain. It will be interesting to find out how chirality in the genus correlates with the temporal and/or spatial left-right asymmetric expression of transcription factors Blimp, Sall and Tbx2/3 identified during Hydroides elegans development (ArenasMena 2008(ArenasMena , 2013.…”

“…3) (Arenas-Mena and Wong, 2007), or the restriction of T-brain to apical tuft sensory precursors ( Fig. 3) (Arenas-Mena, 2008). In general, transcription factor gene expression declines before differentiation, which prevents its unambiguous correlation with larval fates.…”

“…The apical tuft is a sensory organ at the animal tip of the trochophore marked by the expression of T-brain (Fig. 3) (Arenas-Mena, 2008). Blimp is expressed in animal-cap cells that could correspond to larval eye precursors (Arenas-Mena, 2008).…”

“…3) (Arenas-Mena, 2008). Blimp is expressed in animal-cap cells that could correspond to larval eye precursors (Arenas-Mena, 2008). Otx is expressed in ciliary band-associated cells that adopt a neural shape and also in cells associated with the putative posterior sensory organ (Nezlin and Voronezhskaya, 2003), just underneath the ciliary band gap (Fig.…”

Indirect development, transdifferentiation and the macroregulatory evolution of metazoans

“…Perhaps, swimming larvae originated early during metazoan evolution in association with sessile adults, which would explain why both motile ctenophores and placozoans are direct developers. Feeding variants of indirectly developing bilaterians could have evolved by shifting gastrulation to early embryogenesis (Rieger 1994;Arenas-Mena 2008), thereby transforming the originally non-feeding larva that was similar to those of extant cnidarians and sponges (Degnan & Degnan 2006). The feeding variants could have evolved once prior to the PDA or independently in protostomes and deuterostomes (Jägersten 1972;Arenas-Mena 2008).…”