Integrated application of multi-omics provides insights into cold stress responses in pufferfish Takifugu fasciatus

Wen, Xintian; Hu, Yadong; Zhang, Xinyu; Wei, Xiaozhen; Wang, Tao; Yin, Shaowu

doi:10.1186/s12864-019-5915-7

Cited by 60 publications

(35 citation statements)

References 72 publications

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“…Extensive mortality of many farmed fish species could be caused by cold weathers in the winter ( Song et al, 2019 ). The transcriptional responses to cold stress have been characterized in numerous model and farmed fish species, such as zebrafish ( Danio rerio ) ( Long et al, 2012 , 2013 , 2015 ), orange-spotted groupers ( Epinephelus coioides ) ( Sun et al, 2019 ), blue tilapia ( Oreochromis aureus ) ( Nitzan et al, 2019 ), pufferfish ( Takifugu fasciatus ) ( Wen et al, 2019 ), yellow drum ( Nibea albiflora ) ( Xu et al, 2018 ), and Atlantic killifish ( Fundulus heteroclitus ) ( Healy et al, 2017 ). These studies shed light on the mechanisms underlying cold acclimation and the resistance to lethal cold stress in fish.…”

Section: Introductionmentioning

confidence: 99%

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

Long

et al. 2020

Front. Genet.

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Properly regulated transcriptional responses to environmental perturbations are critical for the fitness of fish. Although gene expression profiles in the tissues of common carp upon cold stress were previously characterized, the transcriptional programs underlying cold acclimation are still not well known. In this study, the ability of three common carp strains including Hebao red carp (HB), Songpu mirror carp (SPM) and Yellow river carp (YR) to establish cold resistance after acclimation to a mild hypothermia stress at 18°C for 24 h was confirmed by measurements of the critical thermal minimums (CTMin). The gene expression profiles of the brain and the heart from these strains under both control and cold-acclimated conditions were characterized with RNA-sequencing. The data of the three common carp strains with different genetic background were combined in the differential gene expression analyses to balance the effects of genetic diversity on gene expression. Marked effects of tissue origins on the cold-induced transcriptional responses were revealed by comparing the differentially expressed gene (DEG) lists of the two tissues. Functional categories including spliceosome and RNA splicing were highly enriched in the DEGs of both tissues. However, steroid biosynthesis was specifically enriched in DEGs of the brain and response to unfolded protein was solely enriched in DEGs of the heart. Consistent with the up-regulation of the genes involved in cholesterol biosynthesis, total cholesterol content of the brain was significantly increased upon cold stress. Moreover, cold-induced alternative splicing (AS) events were explored and AS of the rbmx (RNA-binding motif protein, X chromosome) gene was confirmed by real-time quantitative PCR. Finally, a core set of cold responsive genes (CRGs) were defined by comparative transcriptomic analyses. Our data provide insights into the transcriptional programs underlying cold acclimation of common carp and offer valuable clues for further investigating the genetic determinants for cold resistance of farmed fish.

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Section: Introductionmentioning

confidence: 99%

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

Long

et al. 2020

Front. Genet.

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“…In recent years, the multi-omics approach (i.e., genomics, transcriptomics, and proteomics) is becoming increasingly popular as it provides a more holistic molecular perspective of a biological system compared to single omics analysis and/or traditional approaches [22]. Many featured studies [23,24] have attempted to use a multi-omics approach to understand the physiological responses of fish (e.g., pufferfish and turbot) under a variety of stressful conditions. These studies have provided broad perspectives and insights.…”

Section: Introductionmentioning

confidence: 99%

Multi-Omics Analysis Provides Novel Insight into Immuno-Physiological Pathways and Development of Thermal Resistance in Rainbow Trout Exposed to Acute Thermal Stress

Roh

Kim

et al. 2020

IJMS

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In recent years, poikilothermic animals such as fish have increasingly been exposed to stressful high-temperature environments due to global warming. However, systemic changes in fish under thermal stress are not fully understood yet at both the transcriptome and proteome level. Therefore, the objective of this study was to investigate the immuno-physiological responses of fish under extreme thermal stress through integrated multi-omics analysis. Trout were exposed to acute thermal stress by raising water temperature from 15 to 25 °C within 30 min. Head-kidney and plasma samples were collected and used for RNA sequencing and two-dimensional gel electrophoresis. Gene enrichment analysis was performed: differentially expressed genes (DEGs) and differentially expressed proteins (DEPs) were identified to interpret the multi-omics results and identify the relevant biological processes through pathway analysis. Thousands of DEGs and 49 DEPs were identified in fish exposed to thermal stress. Most of these genes and proteins were highly linked to DNA replication, protein processing in the endoplasmic reticulum, cell signaling and structure, glycolysis activation, complement-associated hemolysis, processing of released free hemoglobin, and thrombosis and hypertension/vasoconstriction. Notably, we found that immune disorders mediated by the complement system may trigger hemolysis in thermally stressed fish, which could have serious consequences such as ferroptosis and thrombosis. However, antagonistic activities that decrease cell-free hemoglobin, heme, and iron might be involved in alleviating the side effects of thermally induced immuno-physiological disorders. These factors may represent the major thermal resistance traits that allow fish to overcome extreme thermal stress. Our findings, based on integration of multi-omics data from transcriptomics and proteomics analyses, provide novel insight into the pathogenesis of acute thermal stress and temperature-linked epizootics.

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“…Bismark [41] was applied to align the methylation data to the reference genome, and swDMR [42] was used to analyze the differentially methylated regions (DMR) through a sliding window method. The process of DMR detection and annotation followed the protocols that were previously reported [15,19]. The correlation analysis of DEG and DMP was performed using the R package ggplot2.…”

Section: Dna Methylation Sequencing and Differential Methylation Analmentioning

confidence: 99%

Multi-omics data reveal genes that are relevant for muscular amino acids in the common carp

Zhu

Zhang

Peng

et al. 2020

Preprint

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Background Fish muscular amino acids are a series of essential nutrients that embrace essential amino acids, branched-chain amino acids and flavorous amino acids. Previous studies have found that amino acids have important physiological effects on fish growth and development, as they are involved in maintaining nitrogen balance and in the formation of enzymes and hormones. Amino acids, such as aspartic acid, glutamic acid, glycine and alanine, that can have a significant effect on fish umami taste are called flavorous amino acids. Nevertheless, the studies on the genetic mechanisms of amino acid metabolism in the common carp (Cyprinus carpio) are still limited. Results The purpose of this study was to examine the divergent patterns at the genomic, transcriptomic and epigenomic levels in fish with different amino acid contents. Genome-wide association analysis using 195 individuals of common carp was conducted, and 62 genes were identified to be associated with glycine, proline, and tyrosine content. RNA-Seq of samples with extreme contents of essential amino acids, branched-chain amino acids and flavorous amino acids was applied using brain, liver and muscle tissues, resulting in 1,643 differentially expressed genes. Whole-genome bisulfite sequencing identified 3,108 genes with differentially methylated promoters. Through the enrichment analysis of transcriptome and DNA methylation results, we screened out a series of enriched pathways associated with amino acid metabolism, including various categories of pathways spanning growth regulation, lipid metabolism, the citrate cycle and other signaling pathways. Integrated studies demonstrated prominent correlations between DGE and DMP for amino acid contents trait in brain and muscle tissues. Conclusion In summary, the multi-omics data revealed candidate genes and pathways correlated with amino acid metabolism. These results will promote the process of the genomic selection and breeding strategy in muscular amino acid contents of fish.

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Integrated application of multi-omics provides insights into cold stress responses in pufferfish Takifugu fasciatus

Cited by 60 publications

References 72 publications

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

Transcriptional Programs Underlying Cold Acclimation of Common Carp (Cyprinus carpio L.)

Multi-Omics Analysis Provides Novel Insight into Immuno-Physiological Pathways and Development of Thermal Resistance in Rainbow Trout Exposed to Acute Thermal Stress

Multi-omics data reveal genes that are relevant for muscular amino acids in the common carp

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