Transcriptome Analysis Reveals the lncRNA-mRNA Co-expression Network Regulating the Aestivation of Sea Cucumber

LncRNAs are long non-coding RNAs that are widely recognized as crucial regulators of gene expression and metabolic control, involved in numerous dormancy-related processes. Aestivation is a common hypometabolism strategy of sea cucumber (Apostichopus japonicus) in response to high-temperature conditions and is typically characterized by the degradation of the intestine and respiratory tree. Although the aestivation process has been extensively studied in sea cucumbers, the role of lncRNAs in the context of aestivation states remains a conspicuous knowledge gap. Here, we identified and characterized 14,711 lncRNAs in A. japonicus and analyzed their differential expression patterns during the aestivation process in the intestine and respiratory tree. The results revealed the physiological differences, especially the metabolic processes, between the intestine and respiratory tree during the aestivation. The co-expression network of lncRNA-mRNA suggested the dominant role of lncRNA in regulating the differential response of the intestine and respiratory trees. Differentially co-expressed factors were significantly enriched in the deep-aestivation stage-specific modules. Conserved co-expressed factors included several transcription factors known to be involved in rhythm regulation, such as Klf2 and Egr1. Furthermore, a specific trans-acting lncRNA (lncrna.1393.1) was identified as a potential regulator of Klf2 and Egr1. Overall, the systematic identification, characterization, and expression analysis of lncRNAs in A. japonicus enhanced our knowledge of long non-coding regulation of aestivation in sea cucumber and provided new clues for understanding the common “toolkit” of dormancy regulatory mechanisms.