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

Junjun Yan,Lianyu Shi,Yong Long,Zongbin Cui,Guodong Ge,Qing Li,Chitao Li,Jing Ren

doi:10.1186/s12864-020-06946-8

Abstract

BackgroundClosely 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 unknown. In this study, we compared transcriptomic profiles of two carp species to identify key factors and pathways for cold tolerance and acclimation.ResultsLarvae of Songpu mirror carp and Barbless carp that were pretreated at 18 °C for 24 h 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.ConclusionsThese 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.

Highlights

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 unknown
We further compared the difference of Songpu mirror carp and Barbless carp in cold acclimation
After pretreatment of 9 dpf larvae at 18 °C for 24 h, 94.91% of Songpu mirror carp larvae and 96.84% of Barbless carp larvae in cold acclimation groups (CA) groups were able to survival at lethal cold stress at 10 °C, while 90.61% of Songpu mirror larvae and 22.12% of Barbless carp larvae in CA group were able to survival at lethal cold stress at 8 °C (Fig. 1d) (Additional file 1), indicating that both Songpu mirror carp and Barbless carp possess the ability of cold acclimation and Songpu mirror carp has a stronger ability of cold acclimation than Barbless carp

Summary

Introduction

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 unknown. Fish living in the Arctic and Antarctic regions have evolved a variety of biochemical and physiological mechanisms, including synthesis of antifreeze proteins (AFP) [7], antifreeze glycoproteins (AFGP) [8, 9] and tubulin [10], and lack of hemoglobin [11] to survive in low temperature environments. Many of closely related fish species including some members of the carp family exhibit distinctive abilities of tolerance to low temperature [14]

Methods

Results

Discussion

Conclusion