Acquisition of glial cells missing 2 Enhancers Contributes to a Diversity of Ionocytes in Zebrafish

Takanori Shono,Daisuke Kurokawa,Masataka Okabe,Tsutomu Miyake,Vincent Laudet

doi:10.1371/journal.pone.0023746

Takanori Shono, Daisuke Kurokawa + Show 3 more

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https://doi.org/10.1371/journal.pone.0023746

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Abstract

Glial cells missing 2 (gcm2) encoding a GCM-motif transcription factor is expressed in the parathyroid in amniotes. In contrast, gcm2 is expressed in pharyngeal pouches (a homologous site of the parathyroid), gills, and H+-ATPase–rich cells (HRCs), a subset of ionocytes on the skin surface of the teleost fish zebrafish. Ionocytes are specialized cells that are involved in osmotic homeostasis in aquatic vertebrates. Here, we showed that gcm2 is essential for the development of HRCs and Na+-Cl− co-transporter–rich cells (NCCCs), another subset of ionocytes in zebrafish. We also identified gcm2 enhancer regions that control gcm2 expression in ionocytes of zebrafish. Comparisons of the gcm2 locus with its neighboring regions revealed no conserved elements between zebrafish and tetrapods. Furthermore, We observed gcm2 expression patterns in embryos of the teleost fishes Medaka (Oryzias latipes) and fugu (Fugu niphobles), the extant primitive ray-finned fishes Polypterus (Polypterus senegalus) and sturgeon (a hybrid of Huso huso × Acipenser ruhenus), and the amphibian Xenopus (Xenopus laevis). Although gcm2-expressing cells were observed on the skin surface of Medaka and fugu, they were not found in Polypterus, sturgeon, or Xenopus. Our results suggest that an acquisition of enhancers for the expression of gcm2 contributes to a diversity of ionocytes in zebrafish during evolution.

Highlights

Developmental evolutionary studies have played an important role in elucidating the molecular mechanisms that give rise to morphological divergence and acquisition of new morphological structures and/ or functions
We showed that gcm2 is essential for the development of H+-ATPase–rich cells (HRCs) and Na+-Cl2 co-transporter–rich cells (NCCCs), another subset of ionocytes in the skin of zebrafish
Zebrafish gcm2 is essential for morphogenesis of ionocytes on the skin surface

Summary

Introduction

Developmental evolutionary studies have played an important role in elucidating the molecular mechanisms that give rise to morphological divergence and acquisition of new morphological structures and/ or functions. These studies have proposed a model for the evolution of a novel morphological structure by modification of temporal and spatial patterns of gene expression; that is, changes in gene regulatory networks by adaptive mutations of transcription factors, including cisregulatory elements [1,2,3]. We focused on the glial cells missing (gcm) family and investigated the evolution of ion-regulating organs in vertebrates that may have evolved by changing the molecular developmental mechanisms of gene regulation of the gcm family. Mouse gcm is expressed in the third pharyngeal pouch and the parathyroid gland that develops from the third pouch and is an essential gene for their development [21]

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