Novel budding mode in Polyandrocarpa zorritensis: a model for comparative studies on asexual development and whole body regeneration

Marta Scelzo,Camille Lejeune,Sophie Pagnotta,Stefano Tiozzo,Pauline Henry,Laurel S Hiebert,Francesco Mastrototaro,Alexandre Alié,Laurent Gilletta

doi:10.1186/s13227-019-0121-x

Abstract

BackgroundIn tunicates, the capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. A recent phylogeny of the family Styelidae revealed an independent acquisition of NED in the colonial species Polyandrocarpa zorritensis and highlighted a novel budding mode. In this paper, we provide the first detailed characterization of the asexual life cycle of P. zorritensis.ResultsBud formation occurs along a tubular protrusion of the adult epidermis, the stolon, in a vascularized area defined as budding nest. The bud arises through a folding of the epithelia of the stolon with the contribution of undifferentiated mesenchymal cells. This previously unreported mode of bud onset leads to the formation of a double vesicle, which starts to develop into a zooid through morphogenetic mechanisms common to other Styelidae. The budding nest can also continue to accumulate nutrients and develop into a round-shaped structure, designated as spherule, which represents a dormant form able to survive low temperatures.ConclusionsTo understand the mechanisms of NED and their evolution, it is fundamental to start from a robust phylogenetic framework in order to select relevant species to compare. The anatomical description of P. zorritensis NED provides the foundation for future comparative studies on plasticity of budding and regeneration in tunicates.

Highlights

In addition to sexual reproduction and embryogenesis, a significant number of metazoan species are able to propagate asexually or regenerate completely and form new bodies through non-embryonic development (NED) [1,2,3]
In order to dissect the mechanisms of budding in ascidians and to understand the acquisition and loss of complex characters such as asexual propagation and whole body regeneration, it is necessary to broaden our knowledge of budding modes among different species, and to compare them in a phylogenetic perspective relying on robust trees
The evagination arches progressively to form a double vesicle (Fig. 1): the outer vesicle derives from the adult epidermis and gives rise to the epidermis of the new zooid, while the inner vesicle derives from the peribranchial epithelium and undergoes morphogenetic changes that eventually give rise to the internal organs of the functional new a Styela b tu ep Botryllus schlosseri pe c

Summary

Introduction

In addition to sexual reproduction and embryogenesis, a significant number of metazoan species are able to propagate asexually or regenerate completely and form new bodies through non-embryonic development (NED) [1,2,3]. One of the most well-studied colonial ascidians belongs to the family Styelidae, Botryllus schlosseri (Pallas 1776). In this species, the bud originates from an evagination and thickening of two epithelia, the peribranchial epithelium and the surrounding epidermis, with the possible participation of mesenchymal cells [17]. The capacity to build an adult body via non-embryonic development (NED), i.e., asexual budding and whole body regeneration, has been gained or lost several times across the whole subphylum. We provide the first detailed characterization of the asexual life cycle of P. zorritensis

Methods

Results

Conclusion