Pattern of fin rays along the antero-posterior axis based on their connection to distal radials

Toshiaki Uemoto,Koji Tamura,Hiroki Hamada,Keiichi Kitajima,Tetsuya Umeda,Yoshitaka Tanaka,Yuki Honda,Minori Shinya,Atsushi Kawakami,Koichi Kawakami,Gembu Abe

doi:10.1186/s40851-019-0145-z

Abstract

BackgroundTeleost paired fins are composed of two endoskeletal domains, proximal and distal radials, and an exoskeletal domain, the fin ray. The zebrafish pectoral fin displays elaborately patterned radials along the anteroposterior (AP) axis. Radials are considered homologous to tetrapod limb skeletons, and their patterning mechanisms in embryonic development are similar to those of limb development. Nevertheless, the pattern along the AP axis in fin rays has not been well described in the zebrafish pectoral fin, although several recent reports have revealed that fin ray development shares some cellular and genetic properties with fin/limb endoskeleton development. Thus, fin ray morphogenesis may involve developmental mechanisms for AP patterning in the fin/limb endoskeleton, and may have a specific pattern along the AP axis.ResultsWe conducted detailed morphological observations on fin rays and their connection to distal radials by comparing intra- and inter-strain zebrafish specimens. Although the number of fin rays varied, pectoral fin rays could be categorized into three domains along the AP axis, according to the connection between the fin rays and distal radials; additionally, the number of fin rays varied in the posterior part of the three domains. This result was confirmed by observation of the morphogenesis process of fin rays and distal radials, which showed altered localization of distal radials in the middle domain. We also evaluated the expression pattern of lhx genes, which have AP patterning activity in limb development, in fin rays and during distal radial development and found these genes to be expressed during morphogenesis in both fin rays and distal radials.ConclusionThe fin ray and its connection to the endoskeleton are patterned along the AP axis, and the pattern along the AP axis in the fin ray and the radial connection is constructed by the developmental mechanism related to AP patterning in the limb/fin bud. Our results indicate the possibility that the developmental mechanisms of fin rays and their connection are comparable to those of the distal element of the limb skeleton.

Highlights

Vertebrates have highly elaborated locomotor appendages, namely, fins and limbs, which are adapted to their habitats
In gt223A, the gene trap construct had integrated within the lhx9 gene (Additional file 2B), and the UAS:GFP reporter was expressed in the anterior part of the fin bud at day 2 (Fig. 5f). lhx9 was expressed in the anterior fin bud mesenchyme at 2 dpf (Additional file 3G–J). lhx9, an ortholog of the lhx9 gene, is expressed in the anterior fin/limb bud mesenchyme in a polyodon and tetrapods [19, 35, 37, 38]. These results suggest that the expression of GFP/Gal4 in these transgenic fish lines reproduces the expression pattern of these fin/limb developmental genes. lhx2 and lhx9 play a role in AP patterning in the limb bud under control of the Shh from the zone of polarizing activity (ZPA) [19, 34,35,36,37,38]; our reporter lines can be used
In this study, we found that zebrafish pectoral fin rays exhibit a pattern along the AP axis, which can be divided into three domains categorized by connection between fin rays and distal radials

Summary

Introduction

Vertebrates have highly elaborated locomotor appendages, namely, fins and limbs, which are adapted to their habitats. Teleost paired fins are composed of two endoskeletal domains, the proximal and distal radials, and an exoskeletal domain, the fin ray, and the zebrafish pectoral fin is a representative appendage among teleost species, from both a morphological and developmental biological perspective. The zebrafish pectoral fin has four proximal radials aligned along the anteroposterior (AP) axis that are articulated distally to 6–8 radials (Fig. 1a-c) [3]. Mesenchymal cells migrating into the apical fold (AF) form the fin rays These fin rays are adjacent to the distal radials at their proximal ends, but the topological relationship between fin rays and distal radials remains obscure [3, 4]. Fin ray morphogenesis may involve developmental mechanisms for AP patterning in the fin/limb endoskeleton, and may have a specific pattern along the AP axis

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Discussion

Conclusion