Transcriptomic profiling revealed key signaling pathways for cold tolerance and acclimation of two carp species

Abstract

Background Closely related species of the carp family ( Cyprinidae ) have evolved distinctive abilities to survive under cold stress, but molecular mechanisms underlying the generation of cold resistance remain largely unknow. In this study, we compared transcriptomic profiles of two carp species to identify key factors and pathways for cold tolerance and acclimation. Results Larvae of Songpu mirror carp and Barbless carp that were pretreated at 18°C for 24 hours significantly improved their survival rates under lethal cold temperature at 8°C or 10°C, indicating that two carp species possess the ability of cold acclimation. However, Songpu mirror carp exhibited stronger abilities of cold tolerance and acclimation than Barbless carp. Transcriptomic profiles of Songpu mirror carp and Barbless carp larvae at 28°C and 18°C were compared during cold acclimation through RNA-seq. Differentially expressed genes that are closely associated with the differences in cold acclimation between two carp species were identified through bioinformatics and Venn's diagram analysis. GO enrichment analysis of these genes indicated that cellular component assembly involved in morphogenesis, secondary alcohol metabolism and drug transport were the most up-regulated biological processes during cold acclimation of Songpu mirror carp. Conversely, positive regulation of macroautophagy, intracellular protein transport, and organonitrogen compound catabolism were the most down-regulated biological processes during cold acclimation of Barbless carp. KEGG enrichment analysis revealed that factors in the FoxO-related signaling pathways are mainly responsible for the development of differences in cold tolerance and acclimation between two carp species since altering the phosphorylation of key proteins in the FoxO-related signaling pathways with inhibitors or an activator significantly decreased the cold tolerance and acclimation of Songpu mirror carp. These data provided key clues for dissection of molecular mechanisms underlying the development of cold tolerance and acclimation in carps. Conclusions These findings indicate that larvae of two carp species possess different abilities of cold tolerance and can build cold acclimation under mild low temperature. Multiple biological processes and FoxO-related signaling pathways are closely associated with the development of differences in cold tolerance and acclimation between two carp species.

Characterization of Biological Pathways Regulating Acute Cold Resistance of Zebrafish

“…However, the JNK was not activated by cold stress and had no functions in regulating cold resistance of zebrafish larvae. This is inconsistent with previous study in common carp ( Cyprinus carpio L.) [ 27 ]. This may be ascribed to the genetic differences between these two species.…”

“…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 ].…”

“…The expression of the scd gene, one of the established marker genes of cold stress was reported to be regulated by miR-29a/122 in the kidney of tilapia [ 33 ]. Activity of the FoxO signaling pathway was associated with the difference in cold resistance between two carp species [ 27 ]. The MAPK signaling pathway, especially the p38 MAPK was found to be activated by cold stress in flesh fly ( Sarcophaga crassipalpis ) [ 34 ], Pacific white shrimp ( Litopenaeus vannamei ) [ 35 ] and mouse ( Mus musculus ) [ 36 ].…”