Comparative Transcriptome Analyses of Gayal (Bos frontalis), Yak (Bos grunniens), and Cattle (Bos taurus) Reveal the High-Altitude Adaptation

Abstract

Gayal and yak are well adapted to the local high-altitude environments, yet the transcriptional regulation difference of the plateau environment among them remains obscure. Herein, cross-tissue and cross-species comparative transcriptome analysis were performed for the six hypoxia-sensitive tissues from gayal, yak, and cattle. Gene expression profiles for all single-copy orthologous genes showed tissue-specific expression patterns. By differential expression analysis, we identified 3020 and 1995 differentially expressed genes (DEGs) in at least one tissue of gayal vs. cattle and yak vs. cattle, respectively. Notably, we found that the adaptability of the gayal to the alpine canyon environment is highly similar to the yak living in the Qinghai-Tibet Plateau, such as promoting red blood cell development, angiogenesis, reducing blood coagulation, immune system activation, and energy metabolism shifts from fatty acid β-oxidation to glycolysis. By further analyzing the common and unique DEGs in the six tissues, we also found that numerous expression regulatory genes related to these functions are unique in the gayal and yak, which may play important roles in adapting to the corresponding high-altitude environment. Combined with WGCNA analysis, we found UQCRC1, COX5A are the shared differentially expression hub genes related to the energy supply of myocardial contraction in the heart-related modules of gayal and yak, and CAPS is a shared differentially hub gene among the hub genes of the lung-related module, which is related to pulmonary artery smooth muscle contraction. Additionally, EDN3 is the unique differentially expression hub gene related to the tracheal epithelium and pulmonary vasoconstriction in the lung of gayal. CHRM2 is a unique differentially expression hub gene that was identified in the heart of yak, which has an important role in the autonomous regulation of the heart. These results provide a basis for further understanding the complex transcriptome expression pattern and the regulatory mechanism of high-altitude domestication of gayal and yak.

Variation in gene expression along an elevation gradient of Rhododendron sanguineum var. haemaleum assessed in a comparative transcriptomic analysis

“…, the greater the elevation span, the greater the number of differentially expressed unigenes ( Figure 2B ). This is consistent with other studies on Potentilla L. ( Ma et al., 2015 ), Bos L. ( Ma et al., 2022a ) and other species of Rhododendron ( Liu et al., 2022b ). In this sense, one could hypothesize that along a mountain cline, with increasing elevation, the stresses caused by environmental factors become more severe, and as adaptation of species to these changing environments additional genes are activated, also known as environmental adaptation ( Sun et al., 2018 ; Wang et al., 2021b ).…”

“…In addition, by comparing the high and low elevational samples of different organs, i.e., late flower buds and early leaf buds, the number of significantly DEUs in their respective comparisons showed a positive correlation with the magnitude of the elevational distance, i.e., the greater the elevation span, the greater the number of differentially expressed unigenes (Figure 2B). This is consistent with other studies on Potentilla L. (Ma et al, 2015), Bos L. (Ma et al, 2022a) and other species of Rhododendron (Liu et al, 2022b). In this sense, one could hypothesize that along a mountain cline, with increasing elevation, the stresses caused by environmental factors become more severe, and as adaptation of species to these changing environments additional genes are activated, also known as environmental adaptation (Sun et al, 2018;Wang et al, 2021b).…”

“…To date, several studies on the adaptation to divergent alpine environments have been carried out on animals (e.g. Sun et al., 2018 ; Hao et al., 2019 ; Qu et al., 2020 ; Ma et al., 2022a ). For plants, a few recent studies have reported the genetic architectures and evolutionary processes driving their adaption along elevational gradients (e.g.…”

Single‐cell transcriptomic survey of cell diversity and functional changes in yak hearts at different altitude

“…Studies of yak heart at the tissue and molecular levels have shown that adaptation to the plateau environment mainly involves changes in metabolism, immune function, and adaptation to hypoxia [26][27][28].…”

The uniqueness and superiority of energy utilization in yaks compared with cattle in the highlands: A review

“…For example, results of genome analysis indicated that the CAMK2B gene function to regulate gastric acid secretion in the rumen would be positively selected in the pathway of volatile fatty acid (VFA) production in yaks ( Allen et al., 2009 ; Weimer et al., 2009 ; Qiu et al., 2012 ). Based on the comparative transcriptome analysis of 6 tissues collected from cattle and yaks, Ma et al. (2021) found that among differential genes related to energy metabolism, TPI1 (triosephosphate isomerase) was up regulated and G6PC (the gene encoding glucose-6-phosphatase) was downregulated.…”