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Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan.

ABSTRACT: The evolutionary and genetic origins of the specialized body plan of flatfish are largely unclear. We analyzed the genomes of 11 flatfish species representing 9 of the 14 Pleuronectiforme families and conclude that Pleuronectoidei and Psettodoidei do not form a monophyletic group, suggesting independent origins from different percoid ancestors. Genomic and transcriptomic data indicate that genes related to WNT and retinoic acid pathways, hampered musculature and reduced lipids might have functioned in the evolution of the specialized body plan of Pleuronectoidei. Evolution of Psettodoidei involved similar but not identical genes. Our work provides valuable resources and insights for understanding the genetic origins of the unusual body plan of flatfishes.

SUBMITTER: Lu Z

PROVIDER: S-EPMC8110480 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan.

Lü Zhenming Z Gong Li L Ren Yandong Y Chen Yongjiu Y Wang Zhongkai Z Liu Liqin L Li Haorong H Chen Xianqing X Li Zhenzhu Z Luo Hairong H Jiang Hui H Zeng Yan Y Wang Yifan Y Wang Kun K Zhang Chen C Jiang Haifeng H Wan Wenting W Qin Yanli Y Zhang Jianshe J Zhu Liang L Shi Wei W He Shunping S Mao Bingyu B Wang Wen W Kong Xiaoyu X Li Yongxin Y

Nature genetics 20210419 5

The evolutionary and genetic origins of the specialized body plan of flatfish are largely unclear. We analyzed the genomes of 11 flatfish species representing 9 of the 14 Pleuronectiforme families and conclude that Pleuronectoidei and Psettodoidei do not form a monophyletic group, suggesting independent origins from different percoid ancestors. Genomic and transcriptomic data indicate that genes related to WNT and retinoic acid pathways, hampered musculature and reduced lipids might have functio ...[more]

PMID: 33875864

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Project description:Molecular phylogenetics and phylogenomics are subject to noise from horizontal gene transfer (HGT) and bias from convergence in macromolecular compositions. Extensive variation in size, structure and base composition of alphaproteobacterial genomes has complicated their phylogenomics, sparking controversy over the origins and closest relatives of the SAR11 strains. SAR11 are highly abundant, cosmopolitan aquatic Alphaproteobacteria with streamlined, A+T-biased genomes. A dominant view holds that SAR11 are monophyletic and related to both Rickettsiales and the ancestor of mitochondria. Other studies dispute this, finding evidence of a polyphyletic origin of SAR11 with most strains distantly related to Rickettsiales. Although careful evolutionary modeling can reduce bias and noise in phylogenomic inference, entirely different approaches may be useful to extract robust phylogenetic signals from genomes. Here we develop simple phyloclassifiers from bioinformatically derived tRNA Class-Informative Features (CIFs), features predicted to target tRNAs for specific interactions within the tRNA interaction network. Our tRNA CIF-based model robustly and accurately classifies alphaproteobacterial genomes into one of seven undisputed monophyletic orders or families, despite great variability in tRNA gene complement sizes and base compositions. Our model robustly rejects monophyly of SAR11, classifying all but one strain as Rhizobiales with strong statistical support. Yet remarkably, conventional phylogenetic analysis of tRNAs classifies all SAR11 strains identically as Rickettsiales. We attribute this discrepancy to convergence of SAR11 and Rickettsiales tRNA base compositions. Thus, tRNA CIFs appear more robust to compositional convergence than tRNA sequences generally. Our results suggest that tRNA-CIF-based phyloclassification is robust to HGT of components of the tRNA interaction network, such as aminoacyl-tRNA synthetases. We explain why tRNAs are especially advantageous for prediction of traits governing macromolecular interactions from genomic data, and why such traits may be advantageous in the search for robust signals to address difficult problems in classification and phylogeny.

Dataset Information

Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan.

Publications

Large-scale sequencing of flatfish genomes provides insights into the polyphyletic origin of their specialized body plan.

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