TY - UNPB
T1 - The little skate genome and the evolutionary emergence of wing-like fin appendages
AU - Marletaz, Ferdinand
AU - Calle-Mustienes, Elisa de la
AU - Acemel, Rafael D.
AU - Nakamura, Tetsuya
AU - Paliou, Christina
AU - Naranjo, Silvia
AU - Martinez-Garcia, Pedro M.
AU - Cases, Ildefonso
AU - Sleight, Victoria A.
AU - Hirschberger, Christine
AU - Marcet-Houben, Marina
AU - Navon, Dina
AU - Andrescavage, Ali
AU - Skvortsova, Ksenia
AU - Duckett, Paul E.
AU - Gonzalez-Rajal, Alvaro
AU - Bogdanovic, Ozren
AU - Gibcus, Johan H.
AU - Yang, Liyan
AU - Gallardo-Fuentes, Lourdes
AU - Sospedra, Ismael
AU - Lopez-Rios, Javier
AU - Darbellay, Fabrice
AU - Visel, Axel
AU - Dekker, Job
AU - Shubin, Neil
AU - Gabaldon, Toni
AU - Tena, Juan J.
AU - Lupianez, Dario G.
AU - Rokhsar, Daniel S.
AU - Gomez-Skarmeta, Jose L.
PY - 2022/3/22
Y1 - 2022/3/22
N2 - 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.
AB - 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.
UR - https://doi.org/10.1101/2022.03.21.485123
U2 - 10.1101/2022.03.21.485123
DO - 10.1101/2022.03.21.485123
M3 - Preprint
BT - The little skate genome and the evolutionary emergence of wing-like fin appendages
PB - bioRxiv
ER -