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.

Pattern of New Gene Origination in a Special Fish Lineage, the Flatfishes

“…Four published high-quality Pleuronectoidei genome assemblies, including starry flounder (P. stellatus, GCA_016801935.1), Japanese flounder (P. olivaceus, GCF_001970005.1), turbot (Scophthalmus maximus) and tongue sole (Cynoglossus semilaevis, GCF_000523025.1) [19], were collected to represent the species in Pleuronectoidei. The genome assembly of turbot was downloaded from the website (https://denovo.cnag.cat/turbot) [21].…”

“…Among teleosts, flatfishes have evolved a very unique body plan, especially for its asymmetric body structure has been of great interest [17,18]. Recently, a relatively complete set of genome data of flatfishes and their outgroup species were published by us [19,20], providing a valuable opportunity to comprehensively identify new genes and investigate their possible roles in the evolution of flatfishes.…”

“…In this study, we defined the gene age using Platichthys stellatus (starry flounder) as the focal species representing the real flatfishes (Pleuronectoidei), which has the highest quality of genome assembly in flatfishes. Traditionally flatfishes include Pleuronectoidei and Psettodoidei species, but here we only consider the Pleuronectoidei, because Pleuronectoidei and Psettodoidei do not form a monophyletic group and Psettodoidei has only one species, Psettodeserumei [19]. We reconstructed the phylogenetic tree and estimated the divergence time in order to identify new genes by the SBP method.…”

Identification of Potential Blind-Side Hypermelanosis-Related lncRNA–miRNA–mRNA Regulatory Network in a Flatfish Species, Chinese Tongue Sole (Cynoglossus semilaevis)

“…Chinese tongue sole (Cynoglossus semilaevis) is a prevalent flatfish species in Chinese aquaculture because of its superior nutritive value and economic significance. Like other flatfishes, tongue sole will undergo morphological metamorphosis with an asymmetrical body plan during the larval stage to adapt to an over-substrate dwelling (benthic) lifestyle in later developmental stages (Chen et al, 2014;Shao et al, 2017;Fox et al, 2018;Lü et al, 2021). After metamorphosis, both eyes move to the same side (i.e., the ocular side), which becomes pigmented (black brown) while the blind side remains unpigmented (pure white) (Kang et al, 2011).…”

The complete mitochondrial genome of Toxotes chatareus (Toxotes; Toxotidae; Carangaria) assembled by the next-generation sequencing data and phylogenetic analysis of Carangaria

“…The species was identified based on morphologic features and COI gene (SequenceID: AP006806.1). The NGS data used in this study was produced by our previous study (Lü et al 2021 ) and could be acquired from the public database NCBI with the accession number SRX8345786. The short reads which were produced from the HiSeq platform were used to assemble the mitogenome by MitoZ software with default parameters (Meng et al 2019 ).…”