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The little skate genome and the evolutionary emergence of wing-like fin appendages

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Item Type:Preprint
Title:The little skate genome and the evolutionary emergence of wing-like fin appendages
Creators Name:Marletaz, F. and de la Calle-Mustienes, E. and Acemel, R.D. and Nakamura, T. and Paliou, C. and Naranjo, S. and Martinez-Garcia, P.M. and Cases, I. and Sleight, V.A. and Hirschberger, C. and Marcet-Houben, M. and Navon, D. and Andrescavage, A. and Skvortsova, K. and Duckett, P.E. and Gonzalez-Rajal, A. and Bogdanovic, O. and Gibcus, J.H. and Yang, L. and Gallardo-Fuentes, L. and Sospedra, I. and Lopez-Rios, J. and Darbellay, F. and Visel, A. and Dekker, J. and Shubin, N. and Gabaldon, T. and Tena, J.J. and Lupianez, D.G. and Rokhsar, D.S. and Gomez-Skarmeta, J.L.
Abstract:Skates are cartilaginous fish whose novel body plan features remarkably enlarged wing-like pectoral fins that allow them to thrive in benthic environments. The molecular underpinnings of this unique trait, however, remain elusive. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins (gene expression, chromatin occupancy and three-dimensional (3D) conformation) we find skate-specific genomic rearrangements that alter the 3D regulatory landscape of genes involved in the planar cell polarity (PCP) pathway. Functional inhibition of PCP signaling resulted in marked reduction of anterior fin size, confirming this pathway as a major contributor of batoid fin morphology. We also identified a fin-specific enhancer that interacts with 3' HOX genes, consistent with the redeployment of Hox gene expression in anterior pectoral fins, and confirmed the potential of this element to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganizations and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.
Keywords:Animals, Zebrafish
Source:bioRxiv
Publisher:Cold Spring Harbor Laboratory Press
Article Number:2022.03.21.485123
Date:22 March 2022
Official Publication:https://doi.org/10.1101/2022.03.21.485123

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