Evidence from ileum and liver transcriptomes of resistance to high-salt and water-deprivation conditions in camel

Abstract

Camels have evolved various resistance characteristics adaptive to their desert habitats. In the present study, we used high-throughput sequencing to investigate stress-induced alternative splicing events as well as different genes involved in resistance to water deprivation and salt absorption in the ileum and liver in Camelus bactrianus. Through association analyses of mRNA, miRNA and lncRNA, we sought to explicate how camels respond to high salt and water scarcity conditions. There were two modes by which genes driven by alternative splicing were enriched to molecular functions, invoking of which was potentially fixed by organ and stress types. With qRT-PCR detection, the differentially expressed MUC6, AQP5, LOC105076960, PKP4, CDH11, TENM1, SDS, LOC105061856, PLIN2 and UPP2 were screened as functionally important genes, along with miR-29b, miR-484, miR-362-5p, miR-96, miR-195, miR-128 and miR-148a. These genes contributed to cellular stress resistance, for instance by reducing water loss, inhibiting excessive import of sodium, improving protective barriers and sodium ion homeostasis, and maintaining uridine content. The underlying competing endogenous RNAs referred to LNC001664, let-7e and LOC105076960 mRNA in ileum, and LNC001438, LNC003417, LNC001770, miR-199c and TENM1 mRNA in liver. Besides competent interpretation to resistance, there may be inspirations for curing human diseases triggered by high-salt intake.

Keywords: Camelus bactrianus; Ileum; Liver; Salt stress; Water-deprivation stress.

Fig. 1

Alternative splicing events in the ileum and liver of camel under salt stress and water-deprivation stress. a Five categories of alternative splicing. b Number of differential AS events in the five AS categories of SSI, WSI, SSL and WSL. c Distribution of -log10 (p value) values of differential AS events in each AS category. d Number of molecular functions enriched by protein-coding genes involving differential AS events. e Number of overlapped molecular functions on intersections of different AS categories. f Incidence of enriched similar molecular function from genes regulated by different AS categories. g Two tendentious modes. AS means alternative splicing. A3SS, A5SS, MXE, RI and SE refer respectively to alternative 3′ splice site, alternative 5′ splice site, mutually exclusive exons, retained intron and skipped exon. SSI, WSI, SSL, and WSL separately indicate ileum under salt stress, ileum under water-deprivation stress, liver under salt stress and liver under water-deprivation stress

Fig. 2

Differential mRNAs, miRNAs and lncRNAs in ileum and liver under salt stress and water-deprivation stress. a Expressed level of mRNA and lncRNA with value of log10(FPKM+ 1), and miRNA with value of log10(TPM + 1). b Number of differential mRNAs, miRNAs and lncRNAs. c Log2(fold change) values of up-regulated mRNAs, miRNAs and lncRNAs and -log2(fold change) values of down-regulated mRNAs, miRNAs and lncRNAs. SSI, WSI, CI, SSL, WSL and CL separately indicate ileum under salt stress, ileum under water-deprivation stress, control ileum, liver under salt stress, liver under water-deprivation stress and control liver

Fig. 3

qRT-PCR detection of candidate water-deprivation resistant genes. Data are presented as mean ± SD. Symbols: *, 0.01 < P < 0.05; **, 0.001 < P < 0.01; ***, P < 0.001

Fig. 4

Bioinformatics analysis for significantly differential (P < 0.05) mRNAs, miRNAs and lncRNAs under stress. a KEGG pathway enrichment based on differential protein-coding genes. b Number of common protein-coding genes between stress groups. c Detailed genes information of differential lncRNAs. d Potential mRNAs, miRNAs and lncRNAs serving ceRNA theory. SSI, WSI, SSL and WSL separately indicate ileum under salt stress, ileum under water-deprivation stress, liver under salt stress and liver under water-deprivation stress

Fig. 5

Weakened sodium ion import and water loss with active energy buffer responding to ambient challenge in camel ileum

Fig. 6

Advanced protective barrier and sodium ion homeostasis, and reduced aerobic respiration contributing on salt resistance in camel liver

Fig. 7

Improved uridine, glucose and lipid metabolism under water-deprivation stress in camel liver