Teleost Hox code defines regional identities competent for the formation of dorsal and anal fins

Author:

Adachi Urara1,Koita Rina1ORCID,Seto Akira2,Maeno Akiteru3ORCID,Ishizu Atsuki1,Oikawa Sae1ORCID,Tani Taisei1ORCID,Ishizaka Mizuki1,Yamada Kazuya1ORCID,Satoh Koumi1,Nakazawa Hidemichi1ORCID,Furudate Hiroyuki1ORCID,Kawakami Koichi4ORCID,Iwanami Norimasa2,Matsuda Masaru2ORCID,Kawamura Akinori1ORCID

Affiliation:

1. Division of Life Science, Graduate School of Science and Engineering, Saitama University, Sakura-ku, Saitama 338-8570, Japan

2. Center for Bioscience Research and Education, Utsunomiya University, Utsunomiya 321-8505, Japan

3. Cell Architecture Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan

4. Laboratory of Molecular and Developmental Biology, National Institute of Genetics, and Department of Genetics, Graduate University for Advanced Studies (SOKENDAI), Mishima, Shizuoka 411-8540, Japan

Abstract

The dorsal and anal fins can vary widely in position and length along the anterior–posterior axis in teleost fishes. However, the molecular mechanisms underlying the diversification of these fins remain unknown. Here, we used genetic approaches in zebrafish and medaka, in which the relative positions of the dorsal and anal fins are opposite, to demonstrate the crucial role of hox genes in the patterning of the teleost posterior body, including the dorsal and anal fins. By the CRISPR-Cas9-induced frameshift mutations and positional cloning of spontaneous dorsalfinless medaka, we show that various hox mutants exhibit the absence of dorsal or anal fins, or a stepwise posterior extension of these fins, with vertebral abnormalities. Our results indicate that multiple hox genes, primarily from hoxc -related clusters, encompass the regions responsible for the dorsal and anal fin formation along the anterior–posterior axis. These results further suggest that shifts in the anterior boundaries of hox expression which vary among fish species, lead to diversification in the position and size of the dorsal and anal fins, similar to how modulations in Hox expression can alter the number of anatomically distinct vertebrae in tetrapods. Furthermore, we show that hox genes responsible for dorsal fin formation are different between zebrafish and medaka. Our results suggest that a novel mechanism has occurred during teleost evolution, in which the gene network responsible for fin formation might have switched to the regulation downstream of other hox genes, leading to the remarkable diversity in the dorsal fin position.

Funder

Ministry of Education, Culture, Sports, Science and Technology

National Institute of Genetics

Publisher

Proceedings of the National Academy of Sciences

Reference59 articles.

1. D. E. Facey, B. W. Bowen, B. B. Collette, G. S. Helfman, The Diversity of Fishes: Biology, Evolution and Ecology (John Wiley & Sons, ed. 3, 2022).

2. P. A. Hastings H. J. Walker Jr. G. R. Galland Fishes: A Guide to Their Diversity (University of California Press 2015).

3. Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data

4. Resolution of ray-finned fish phylogeny and timing of diversification

5. J. S. Nelson T. C. Grande M. V. H. Eilson Fishes of the World (Wiley ed. 5 2016).

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