Development, organization, and remodeling of phoronid muscles from embryo to metamorphosis (Lophotrochozoa: Phoronida).

Elena N Temereva,Eugeni B Tsitrin

doi:10.1186/1471-213x-13-14

Abstract

BackgroundThe phoronid larva, which is called the actinotrocha, is one of the most remarkable planktotrophic larval types among marine invertebrates. Actinotrochs live in plankton for relatively long periods and undergo catastrophic metamorphosis, in which some parts of the larval body are consumed by the juvenile. The development and organization of the muscular system has never been described in detail for actinotrochs and for other stages in the phoronid life cycle.ResultsIn Phoronopsis harmeri, muscular elements of the preoral lobe and the collar originate in the mid-gastrula stage from mesodermal cells, which have immigrated from the anterior wall of the archenteron. Muscles of the trunk originate from posterior mesoderm together with the trunk coelom. The organization of the muscular system in phoronid larvae of different species is very complex and consists of 14 groups of muscles. The telotroch constrictor, which holds the telotroch in the larval body during metamorphosis, is described for the first time. This unusual muscle is formed by apical myofilaments of the epidermal cells. Most larval muscles are formed by cells with cross-striated organization of myofibrils. During metamorphosis, most elements of the larval muscular system degenerate, but some of them remain and are integrated into the juvenile musculature.ConclusionEarly steps of phoronid myogenesis reflect the peculiarities of the actinotroch larva: the muscle of the preoral lobe is the first muscle to appear, and it is important for food capture. The larval muscular system is organized in differently in different phoronid larvae, but always exhibits a complexity that probably results from the long pelagic life, planktotrophy, and catastrophic metamorphosis. Degeneration of the larval muscular system during phoronid metamorphosis occurs in two ways, i.e., by complete or by incomplete destruction of larval muscular elements. The organization and remodeling of the muscular system in phoronids exhibits the combination of protostome-like and deuterostome-like features. This combination, which has also been found in the organization of some other systems in phoronids, can be regarded as an important characteristic and one that probably reflects the basal position of phoronids within the Lophotrochozoa.

Highlights

The phoronid larva, which is called the actinotrocha, is one of the most remarkable planktotrophic larval types among marine invertebrates
Myogenesis Muscle cells differentiate from mesodermal cells, which have immigrated from the anterior ectodermal–endodermal boundary in the mid-gastrula stage (Figure 1A)
The muscular system consists of the continuous layer of the cells above the blastopore

Summary

Introduction

The phoronid larva, which is called the actinotrocha, is one of the most remarkable planktotrophic larval types among marine invertebrates. New data on protostomian features in phoronid embryology have recently been published [4], these results do not allow the definite establishment of phoronids as typical protostomian animals [5]. The obtaining of new and detailed information about phoronid development will help answer questions about the phoronid phylogeny. For example, the arrangement of muscles is metameric after metamorphosis but is mesh-like before metamorphosis [6,7]. This suggests the absence of metamery in the common bilaterian ancestor [6,7]

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