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

Abstract

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.

Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations

“…Among them, DDX23 harboring a synonymous variant with the lowest sum of ranks shows an almost 2.5-fold transcriptional upregulation in tropically adapted Sahiwal cattle in comparison to high-altitude adapted Ladakhi cattle [29]. Additionally, DDX23 is upregulated under cold stress in common carp (Cyprinus carpio L.) and belongs to core cold response genes in this species [30]. Although synonymous codon substitutions do not lead to amino acid change, they could affect the cellular level of coded protein or, in some cases, its structure [45] or be linked to genetic variants of other types.…”

Characterization of Biological Pathways Regulating Acute Cold Resistance of Zebrafish

“…Quantitative real-time PCR (qPCR) was performed as previously described to validate the results of RNA-seq [ 18 ]. Expression of genes including fosab , foxq1a , npas4a , etc., was analyzed by qPCR.…”

“…Furthermore, stress responses can result in acclimation to the changed temperature, extend the thermal breadth and thus enhance the thermal tolerance of fish [ 15 , 16 ]. Acclimation of fish to mild cold stress was previously reported to significantly improve resistance to subsequent severe cold stresses [ 17 , 18 ]. Thus, responses of fish to cold stress have attracted intensive research interests in recent years and alterations in organismal physiology, secretion of hormones, subcellular structures, cellular biochemical compositions, transcriptome profiles, protein post-translational modifications and concentration of metabolites upon exposure to cold stress have been reported [ 19 , 20 , 21 , 22 , 23 , 24 , 25 ].…”

“…These studies identified numerous cold responsive genes (CRGs) from fish including both research models and farmed species. Genes such as the cold-inducible RNA binding protein ( cirbp ), high mobility group box ( hmgb ) and stearoyl-CoA desaturase ( scd ) were revealed to be the marker genes induced by cold stress [ 17 , 18 , 21 , 27 ]. Many CRGs demonstrate no changes in overall abundance but undergo alternative splicing upon cold stress [ 28 , 29 ].…”

Effects of Bile Acids Supplement in High Plant Protein Diet on Common Carp (Cyprinus Carpio) Bile Acids Profile and Hepatopancreas Health

“…Common carp [30] is a kind of omnivorous fish, an important economical freshwater fish in China. It needs a certain amount of animal protein, and a high proportion of plant protein may cause intestinal and liver diseases, thereby reducing the benefit of breeding.…”