When the tap runs dry: The multi-tissue gene expression and physiological responses of water deprived Peromyscus eremicus

Abstract

The harsh and dry conditions of desert environments have resulted in genomic adaptations, allowing for desert organisms to withstand prolonged drought, extreme temperatures, and limited food resources. Here, we present a comprehensive exploration of gene expression across five tissues (kidney, liver, lung, gastrointestinal tract, and hypothalamus) and 19 phenotypic measurements to explore the whole-organism physiological and genomic response to water deprivation in the desert-adapted cactus mouse (Peromyscus eremicus). The findings encompass the identification of differentially expressed genes and correlative analysis between phenotypes and gene expression patterns across multiple tissues. Specifically, we found robust activation of the vasopressin renin-angiotensin-aldosterone system (RAAS) pathways, whose primary function is to manage water and solute balance. Animals reduce food intake during water deprivation, and upregulation of PCK1 highlights the adaptive response to reduced oral intake via its actions aimed at maintained serum glucose levels. Even with such responses to maintain water balance, hemoconcentration still occurred, prompting a protective downregulation of genes responsible for the production of clotting factors while simultaneously enhancing angiogenesis which is thought to maintains tissue perfusion. In this study, we elucidate the complex mechanisms involved in water balance in the desert-adapted cactus mouse, P. eremicus. By prioritizing a comprehensive analysis of whole-organism physiology and multi-tissue gene expression in a simulated desert environment, we describe the complex and successful response of regulatory processes.

Keywords: Peromyscus; RNAseq; dehydration; multi-tissue; physiology.

Figure 1

Log2FC of all genes across the lung (lu), liver (liv), gastrointestinal tract (gi), hypothalamus (hyp), and kidney (kid) of Peromyscus eremicus with water vs without water. Blue and green colored dots indicate p<0.05, whereas grey dots indicate p>=0.05.

Figure 2

Visualization of gene ontology (GO) terms to show common WGCNA modules within and between the lung (lu), liver (liv), gastrointestinal tract (gi), hypothalamus (hyp), and kidney (kid) of Peromyscus eremicus. Visualized are selections of the top 20 significant GO terms for each phenotype module combination. The number of genes in the GO term are indicated by size of the dots.

Figure 3

Canonical correspondence analysis (CCA) indicates correlations between normalized differentially expressed genes and physiological measurements for Peromyscus eremicus with and without access to water. The distribution of tissue samples in Euclidian space as a function of their gene expression values is shown (points colored by tissue type and water treatment). Outlier genes (defined as two standard deviations or more from the mean) are colored blue. Inlier genes (defined as less than two standard deviations from the mean) are colored grey. CCA reveals a significant relationship between proportion weight loss (F = 4.8006, P = 0.001) and, while not significant, a strong relationship for water loss rate (WLR) (F = 1.9856, P = 0.096). This can be seen by a subset of genes (blue) pulled in the direction of the proportion weight loss (pro_weight) ordination vector and a subset of genes (blue) pulled in the direction of the WLR (mean_H₂Og) ordination vector.