Abstract

BackgroundPax genes are transcription factors with significant roles in cell fate specification and tissue differentiation during animal ontogeny. Most information on their tempo-spatial mode of expression is available from well-studied model organisms where the Pax-subfamilies Pax2/5/8, Pax6, and Paxα/β are mainly involved in the development of the central nervous system (CNS), the eyes, and other sensory organs. In certain taxa, Pax2/5/8 seems to be additionally involved in the development of excretion organs. Data on expression patterns in lophotrochozoans, and in particular in mollusks, are very scarce for all the above-mentioned Pax-subfamilies, which hampers reconstruction of their putative ancestral roles in bilaterian animals. Thus, we studied the developmental expression of Pax2/5/8, Pax6, and the lophotrochozoan-specific Paxβ in the worm-shaped mollusk Wirenia argentea, a member of Aplacophora that together with Polyplacophora forms the Aculifera, the proposed sister taxon to all primarily single-shelled mollusks (Conchifera).ResultsAll investigated Pax genes are expressed in the developing cerebral ganglia and in the ventral nerve cords, but not in the lateral nerve cords of the tetraneural nervous system. Additionally, Pax2/5/8 is expressed in epidermal spicule-secreting or associated cells of the larval trunk and in the region of the developing protonephridia. We found no indication for an involvement of the investigated Pax genes in the development of larval or adult sensory organs of Wirenia argentea.ConclusionsPax2/5/8 seems to have a conserved role in the development of the CNS, whereas expression in the spicule-secreting tissues of aplacophorans and polyplacophorans suggests co-option in aculiferan skeletogenesis. The Pax6 expression pattern in Aculifera largely resembles the common bilaterian expression during CNS development. All data available on Paxβ expression argue for a common role in lophotrochozoan neurogenesis.

Highlights

  • paired box (Pax) genes are transcription factors with significant roles in cell fate specification and tissue differentiation during animal ontogeny

  • Larval morphology of the neomeniomorph Wirenia argentea Wirenia argentea develops via a lecithotrophic trochophorelike larva, the so-called pericalymma or test cell larva

  • These play a crucial role in the development and regionalization of the highly centralized and complex brains of vertebrates and insects as well as cephalopods, where they were most likely independently recruited into similar functions [24, 27]

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Summary

Introduction

Pax genes are transcription factors with significant roles in cell fate specification and tissue differentiation during animal ontogeny. Two lateral (visceral) nerve cords emanate from the cerebral ganglion, while the pedal ganglia give rise to a pair of ventral (pedal) nerve cords Together, these four longitudinal nerve cords form the Scherholz et al BMC Evolutionary Biology (2017) 17:81 molluscan tetraneural nervous system [6,7,8,9,10] (see Fig. 1). Before the tetraneural condition is established, two longitudinal neurite bundles emerge simultaneously from both the anterior and the posterior pole and subsequently fuse in the region of the prototroch, the locomotive ciliary band of the free-swimming larva [13] (Fig. 1a) This formation of an intermediate stage with a single pair of nerve cords has recently been interpreted as a putative ancestral feature of spiralian neurogenesis [13]

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