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小鳐鱼基因组与翼状鳍的进化起源。

The little skate genome and the evolutionary emergence of wing-like fins.

机构信息

Centre for Life's Origin and Evolution, Department of Genetics, Evolution and Environment, University College London, London, UK.

Molecular Genetics Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Japan.

出版信息

Nature. 2023 Apr;616(7957):495-503. doi: 10.1038/s41586-023-05868-1. Epub 2023 Apr 12.

Abstract

Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments. However, the molecular underpinnings of this unique trait remain unclear. 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-including gene expression, chromatin occupancy and three-dimensional conformation-we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.

摘要

鳐鱼是软骨鱼类,其身体形态特征为增大的翼状胸鳍,使它们能够在底层环境中茁壮成长。然而,这种独特特征的分子基础仍不清楚。在这里,我们通过开发小鳐鱼 Leucoraja erinacea 作为基因组功能模型来研究这种表型创新的起源。对小鳐鱼高质量染色体规模基因组序列的分析表明,与其他测序基因组相比,它保留了许多古老的有颌脊椎动物特征,包括许多古老的微染色体。将基因组比较与发育中的鳍的广泛调控数据集(包括基因表达、染色质占据和三维构象)相结合,我们发现了鳐鱼特有的基因组重排,改变了参与平面细胞极性途径的基因的三维调控景观。平面细胞极性信号的功能抑制导致前鳍尺寸减小,证实该途径是 batoid 鳍形态的主要贡献者。我们还鉴定了一个鳍特异性增强子,它与几个 hoxa 基因相互作用,与 hox 基因在前胸鳍中的重新表达一致,并通过斑马鱼报告基因检测证实了其在前面鳍中激活转录的潜力。我们的研究结果强调了基因组重组和调控变异在表型进化中的核心作用,揭示了一个神秘特征的分子起源。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/3b85/10115646/aab73818fcfa/41586_2023_5868_Fig1_HTML.jpg

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