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Comparative Physiological and Transcriptomic Profiling Offers Insight into the Sexual Dimorphism of Hepatic Metabolism in Size-Dimorphic Spotted Scat (Scatophagus argus).

ABSTRACT: The spotted scat (Scatophagus argus) is an economically important cultured marine fish that exhibits a typical sexual size dimorphism (SSD). SSD has captivated considerable curiosity for farmed fish production; however, up till now the exact underlying mechanism remains largely unclear. As an important digestive and metabolic organ, the liver plays key roles in the regulation of fish growth. It is necessary to elucidate its significance as a downstream component of the hypothalamic-pituitary-liver axis in the formation of SSD. In this study, the liver physiological differences between the sexes were evaluated in S. argus, and the activity of several digestive and metabolic enzymes were affected by sex. Females had higher amylase, protease, and glucose-6-phosphate dehydrogenase activities, while males exhibited markedly higher hepatic lipase and antioxidant enzymes activities. A comparative transcriptomics was then performed to characterize the responsive genes. Illumina sequencing generated 272.6 million clean reads, which were assembled into 79,115 unigenes. A total of 259 differentially expressed genes were identified and a few growth-controlling genes such as igf1 and igfbp1 exhibited female-biased expression. Further analyses showed that several GO terms and pathways associated with metabolic process, particularly lipid and energy metabolisms, were significantly enriched. The male liver showed a more active mitochondrial energy metabolism, implicating an increased energy expenditure associated with reproduction. Collectively, the female-biased growth dimorphism of S. argus may be partially attributed to sexually dimorphic metabolism in the liver. These findings would facilitate further understanding of the nature of SSD in teleost fish.

SUBMITTER: Chen H

PROVIDER: S-EPMC8233746 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Unlike mammals and birds, many fishes have young sex chromosomes, providing excellent models to study sex chromosome differentiation at early stages. Previous studies showed that spotted scat possesses an XX-XY sex determination system. The X has a complete Dmrt3 copy (termed normal) and a truncated copy of Dmrt1 (called Dmrt1b), while the Y has the opposite (normal Dmrt1, which is male-specific, and a truncated Dmrt3 called Dmrt3△-Y). Dmrt1 is the candidate sex determination gene, while the differentiation of other sex-linked genes remains unknown. The spotted scat has proven to be a good model to study the evolution of sex chromosomes in vertebrates. Herein, we sequenced a neighbor gene of this family, Dmrt2, positioned farther from Dmrt1 and closer to Dmrt3 in the spotted scat, and analyzed its sequence variation and expression profiles. The physical locations of the three genes span across an estimated size of >40 kb. The open reading frames of Dmrt2a and its paralog Dmrt2b are 1578 bp and 1311 bp, encoding peptides of 525 and 436 amino acid residues, respectively. Dmrt2a is positioned close to Dmrt3 but farther from Dmrt1 on the same chromosome, while Dmrt2b is not. Sequence analysis revealed several mutations; insertions, and deletions (indels) on Dmrt2a non-coding regions and single-nucleotide polymorphisms (SNPs) on the Dmrt2a transcript. These indels and SNPs are sex-linked and showed high male heterogeneity but do not affect gene translation. The markers designed to span the mutation sites tested on four different populations showed varied concordance with the genetic sexes. Dmrt2a is transcribed solely in the gonads and gills, while Dmrt2b exists in the gonads, hypothalamus, gills, heart, and spleen. The Dmrt2a and Dmrt2b transcripts are profoundly expressed in the male gonads. Analyses of the transcriptome data from five other fish species (Hainan medaka (Oryzias curvinotus), silver sillago (Sillago sihama), Nile tilapia (Oreochromis niloticus), Hong Kong catfish (Clarias fuscus), and spot-fin porcupine fish (Diodon hystrix)) revealed testes-biased expression of Dmrt1 in all, similar to spotted scat. Additionally, the expression of Dmrt2a is higher in the testes than the ovaries in spotted scat and Hainan medaka. The Dmrt2a transcript was not altered in the coding regions as found in Dmrt1 and Dmrt3 in spotted scat. This could be due to the functional importance of Dmrt2a in development. Another possibility is that because Dmrt2a is positioned farther from Dmrt1 and the chromosome is still young, meaning it is only a matter of time before it differentiates. This study undeniably will aid in understanding the functional divergence of the sex-linked genes in fish.

Project description:BACKGROUND:Scatophagus argus is a popular farmed fish in several countries of Southeast Asia, including China. Although S. argus has a highly promising economic value, a significant lag of breeding research severely obstructs the sustainable development of aquaculture industry. As one of the most important economic traits, growth traits are controlled by multiple gene loci called quantitative trait loci (QTLs). It is urgently needed to launch a marker assisted selection (MAS) breeding program to improve growth and other pivotal traits. Thus a high-density genetic linkage map is necessary for the fine mapping of QTLs associated with target traits. RESULTS:Using restriction site-associated DNA sequencing, 6196 single nucleotide polymorphism (SNP) markers were developed from a full-sib mapping population for genetic map construction. A total of 6193 SNPs were grouped into 24 linkage groups (LGs), and the total length reached 2191.65 cM with an average marker interval of 0.35 cM. Comparative genome mapping revealed 23 one-to-one and 1 one-to-two syntenic relationships between S. argus LGs and Larimichthys crocea chromosomes. Based on the high-quality linkage map, a total of 44 QTLs associated with growth-related traits were identified on 11 LGs. Of which, 19 significant QTLs for body weight were detected on 9 LGs, explaining 8.8-19.6% of phenotypic variances. Within genomic regions flanking the SNP markers in QTL intervals, we predicted 15 candidate genes showing potential relationships with growth, such as Hbp1, Vgll4 and Pim3, which merit further functional exploration. CONCLUSIONS:The first SNP genetic map with a fine resolution of 0.35 cM for S. argus has been developed, which shows a high level of syntenic relationship with L. crocea genomes. This map can provide valuable information for future genetic, genomic and evolutionary studies. The QTLs and SNP markers significantly associated with growth-related traits will act as useful tools in gene mapping, map-based cloning and MAS breeding to speed up the genetic improvement in important traits of S. argus. The interesting candidate genes are promising for further investigations and have the potential to provide deeper insights into growth regulation in the future.

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Comparative Physiological and Transcriptomic Profiling Offers Insight into the Sexual Dimorphism of Hepatic Metabolism in Size-Dimorphic Spotted Scat (Scatophagus argus).

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