Adipose gene expression profiles reveal novel insights into the adaptation of northern Eurasian semi-domestic reindeer (Rangifer tarandus)

Abstract

Reindeer (Rangifer tarandus) are semi-domesticated animals adapted to the challenging arctic conditions of northern Eurasia. Adipose tissues play a crucial role in animals living in northern environments by altering gene expression in their tissues to regulate energy homeostasis and thermogenic activity. Here, we performed transcriptome profiling by RNA sequencing of adipose tissues from three different anatomical depots: metacarpal (bone marrow), perirenal, and prescapular fat in Finnish and Even reindeer (in Sakha) during two seasonal time points (spring and winter). On average 36.5 million pair-ended clean reads were obtained for each sample, and a total of 16,362 genes were expressed in our data. Gene expression profiles in metacarpal tissue were distinct and clustered separately from perirenal and prescapular adipose tissues. Notably, metacarpal adipose tissue appeared to have a significant role in the regulation of the energy metabolism of reindeer in spring when their nutritional condition is poor after winter. During spring, when the animals are in less optimal condition, genes associated with the immune system (e.g., CCL2, CCL11, CXCL14, IGSF3, IGHM, IGLC7, IGKC, JCHAIN, and IGSF10) were upregulated in the perirenal and prescapular adipose tissue, while genes involved in energy metabolism (e.g., ACOT2, APOA1, ANGPTL1, ANGPTL8, ELOVL7, MSMO1, PFKFB1, and ST3GAL6) were upregulated in metacarpal tissue. Even reindeer harboured relatively fewer significantly differentially expressed genes than Finnish reindeer, irrespective of the season, possibly owing to climatic and management differences. Moreover, blood and tissue parameters reflecting general physiological and metabolic status showed less seasonal variation in Even reindeer than in Finnish reindeer. This study identified adipose candidate genes potentially involved in immune response, fat deposition, energy metabolism, development, cell growth, and organogenesis. Taken together, this study provides new information on the mechanisms by which reindeer adapt to less optimal arctic conditions.

Whole-Genome Resequencing Points to Candidate DNA Loci Affecting Body Temperature under Cold Stress in Siberian Cattle Populations

“…For some genes, we found additional evidence in species phylogenetically close to cattle. For example, according to Swain and colleagues, variations in TMBIM6 affect the rectal temperature in Indian goats [48], while FKBP11 is a candidate for involvement in seasonal adaptations in reindeer (Rangifer tarandus) [49]. There are several genes that are related to thermoregulation or cold adaptation in non-ungulate species.…”

Adipose gene expression profiles and their associations with adaptations in Northern Finncattle, Mirandesa cattle, Yakutian cattle and Holstein cattle

“…White adipose tissue stores energy, whereas brown adipose tissue dissipates stored energy as heat by burning fatty acids to maintain body temperature [9]. Fat in bone marrow acts as an energy reservoir contributing to metabolic processes and undergoes dynamic changes, for example, as a result of starvation [10].…”

“…Fat in bone marrow acts as an energy reservoir contributing to metabolic processes and undergoes dynamic changes, for example, as a result of starvation [10]. Weldenegodguad et al [9] recently reported that the gene expression profiles of metacarpal tissues were distinct from those of perirenal and prescapular fats in semi-domestic reindeer (Rangifer tarandus), providing interesting insights into the nature of adipose tissues, with candidate genes involved in immune response and energy metabolism.…”

“…The native cattle breeds included in this study have adapted to various biogeographical and production environments and have different genetic origins and breeding histories-Mirandesa cattle from Portugal, Northern Finncattle from Finland and Yakutian cattle from the Sakha Republic (Yakutia), the Russian Federation. In addition, we investigated the Holstein cattle breed, which is the high-producing and most popular dairy cattle breed worldwide (Figure 1) [3,9]. Studying the genetic resources of native, locally adapted cattle is essential due to climate change; the current productive commercial breeds, such as the 5 Holstein breed, may not express the genetic variations important for future breeding and adaptation to changing environments [11].…”

“…Studying the genetic resources of native, locally adapted cattle is essential due to climate change; the current productive commercial breeds, such as the 5 Holstein breed, may not express the genetic variations important for future breeding and adaptation to changing environments [11]. Yakutian cattle, for example, live in the area of Sakha (Yakutia), which has some of the most extreme low temperatures in the settled world (-70°C to +30°C); thus, this breed is of great interest when studying adaptation to cold [2,9]. Adaptation to cold temperatures simultaneously implies adaptation to a different type of diet, which in this case consists of wild forage.…”