Comparative analysis of the microRNA transcriptome between yak and cattle provides insight into high-altitude adaptation

Guan, Jiuqiang; Long, Keren; Ma, Jideng; Zhang, Jinwei; He, Dafang; Jin, Long; Tang, Qianzi; Jiang, Anan; Wang, Xun; Hu, Yaodong; Tian, Shilin; Jiang, Zhi; Li, Mingzhou; Luo, Xiaolin

doi:10.7717/peerj.3959

Cited by 50 publications

(58 citation statements)

References 52 publications

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“…Further, miR-29a-3p expression is increased in heart and muscle of adults versus pups, which is predicted to decrease expression of Hif3a and Vhl, both negative regulators of hypoxia signal transduction by HIF1α. Similar miRNA targeting of hypoxia signaling pathways was highlighted as an adaptation to high altitude in the yak, however a distinct set of miR-NAs of interest were identified [20].…”

Section: Regulation Of Hypoxia Tolerancementioning

confidence: 91%

“…MiRNAs appear critical to the development of tissue-specific phenotypes and evolutionary adjustments in gene expression [18,19]. For example, differential miRNA profiles in the highland yak compared to the lowland cow are enriched for hypoxia signaling pathways in the respiratory and cardiovascular systemsa key component of altitude adaptation [20]. These small non-coding RNAs also regulate seasonal phenotypic shifts, including metabolic depression that accompanies hibernation, anoxia tolerance and estivation in several vertebrates, although the exact miRNAs that may regulate these transitions appear speciesspecific [21,22].…”

Section: Introductionmentioning

confidence: 99%

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microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation

et al. 2020

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Background: The Weddell Seal (Leptonychotes weddelli) represents a remarkable example of adaptation to diving among marine mammals. This species is capable of diving > 900 m deep and remaining underwater for more than 60 min. A number of key physiological specializations have been identified, including the low levels of aerobic, lipid-based metabolism under hypoxia, significant increase in oxygen storage in blood and muscle; high blood volume and extreme cardiovascular control. These adaptations have been linked to increased abundance of key proteins, suggesting an important, yet still understudied role for gene reprogramming. In this study, we investigate the possibility that post-transcriptional gene regulation by microRNAs (miRNAs) has contributed to the adaptive evolution of diving capacities in the Weddell Seal. Results: Using small RNA data across 4 tissues (brain, heart, muscle and plasma), in 3 biological replicates, we generate the first miRNA annotation in this species, consisting of 559 high confidence, manually curated miRNA loci. Evolutionary analyses of miRNA gain and loss highlight a high number of Weddell seal specific miRNAs. Four hundred sixteen miRNAs were differentially expressed (DE) among tissues, whereas 80 miRNAs were differentially expressed (DE) across all tissues between pups and adults and age differences for specific tissues were detected in 188 miRNAs. mRNA targets of these altered miRNAs identify possible protective mechanisms in individual tissues, particularly relevant to hypoxia tolerance, anti-apoptotic pathways, and nitric oxide signal transduction. Novel, lineage-specific miRNAs associated with developmental changes target genes with roles in angiogenesis and vasoregulatory signaling.Conclusions: Altogether, we provide an overview of miRNA composition and evolution in the Weddell seal, and the first insights into their possible role in the specialization to diving.

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Section: Regulation Of Hypoxia Tolerancementioning

confidence: 91%

Section: Introductionmentioning

confidence: 99%

microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation

et al. 2020

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Section: Regulation Of Hypoxia Tolerancementioning

confidence: 94%

“…MiRNAs appear critical to the development of tissue-specific phenotypes and evolutionary adjustments in gene expression [18,19]. For example, differential miNAR profiles in the highland yak compared to the lowland cow are enriched for hypoxia signaling pathways in the respiratory and cardiovascular systems -a key component of altitude adaptation [20]. These small non-coding RNAs also regulate seasonal phenotypic shifts, including metabolic depression that accompanies hibernation, anoxia tolerance and estivation in several vertebrates, although the exact miRNAs that may regulate these transitions appear species-specific [21,22].…”

Section: Introductionmentioning

confidence: 99%

microRNA profiling in the Weddell Seal suggests novel regulatory mechanisms contributing to diving adaptation

Penso-Dolfin

Haerty

Hindle

et al. 2019

Preprint

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ABSTRACTThe Weddell Seal (Leptonychotes weddelli) represents a remarkable example of adaptation to diving among marine mammals. This species is capable of diving >900 m deep and remaining underwater for more than 60 minutes. A number of key physiological specializations have been identified, including the low levels of aerobic, lipid-based metabolism under hypoxia, significant increase in oxygen storage in blood and muscle; high blood volume and extreme cardiovascular control. These adaptations have been linked to increased abundance of key proteins, suggesting an important, yet still understudied role for gene reprogramming.In this study, we investigate the possibility that post-transcriptional gene regulation by microRNAs (miRNAs) has contributed to the adaptive evolution of diving capacities in the Weddell Seal.Using small RNA data across 4 tissues (cortex, heart, muscle and plasma), in 3 biological replicates, we generate the first miRNA annotation in this species, consisting of 559 high confidence, manually curated miRNA loci. Evolutionary analyses of miRNA gain and loss highlight a high number of Weddell seal specific miRNAs.416 miRNAs were differentially expressed (DE) among tissues, whereas 83 miRNAs were differentially expressed (DE) across all tissues between pups and adults and 221 miRNAs demonstrated developmental changes in specific tissues only. mRNA targets of these altered miRNAs identify possible protective mechanisms in individual tissues, particularly relevant to hypoxia tolerance, anti-apoptotic pathways, and nitric oxide signal transduction. Novel, lineage-specific miRNAs associated with developmental changes target genes with roles in angiogenesis and vasoregulatory signaling.Altogether, we provide an overview of miRNA composition and evolution in the Weddell seal, and the first insights into their possible role in the specialization to diving.

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“…Hence, it is necessary not only to use the migration and low-altitude cattle to study the hypoxic adaptation mechanism, but also to use yak. Recent studies on morphology [8], anatomy [9], physiology [10], genomics [3], mRNA [11][12] and small RNAs [13] of yak have focused on the high-altitude adaptation mechanism, but limited researches are centered on the whole transcriptome and their regulatory network in high altitude adaptation.…”

mentioning

confidence: 99%

Whole-transcriptome analysis of heart in bovidae reveals regulatory pathways associated with high-altitude adaptation

Wang¹,

Chai²,

Zhong³

et al. 2019

Preprint

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Background: the yak (Bos grunniens) is one of the major livestock that can survive the extremely cold, harsh and oxygen-poor conditions and provide meat, milk and transportation for Tibetans living in the Qinghai-Tibetan Plateau, and there are some cattle migrate to yak habitat but cannot survive the extremely conditions well. However, the regulatory mechanisms that drive hypoxic adaptation of yak remain elusive. Results: Thus, we collected heart tissues from Leiwuqi (LWQ) yak and their relatives, the migration cattle in LWQ yak habitat (HAC) and low-altitude cattle (LAC), respectively, for RNA sequencing, 178 co-differentially expressed protein-coding transcripts (CETs) including 6 down-regulated and 172 up-regulated CETs were discovered in both LAC-vs-LWQY and LAC-vs-HAC comparison groups. There were 133, 11 and 3 lncRNA transcripts were specific expressed in LWQY, HAC, and LAC groups, respectively. 2 and 230 lncRNA transcripts differentially expressed in LAC-vs-LWQY and LAC-vs-HAC，respectively, but no lncRNA transcripts co-differentially expressed in those two comparison groups. Among the 58 miRNAs that were co-differentially expressed, 18 were up-regulated and 40 were down-regulated. In addition, 640 (501 up-regulated and 139 down-regulated) and 152 (152 up-regulated and 1 down-regulated) circRNAs showed differential expression in LAC-vs-LWQY and LAC-vs-HAC comparison groups, respectively, and 53 up-regulated co-differentially expressed circRNAs were shared. Multiply CETs which are the target genes for miRNAs/lncRNAs were significantly enriched in high-altitude adaptation related processes, for instance, T cell receptor signaling, VEGF signaling, and cAMP signaling. A competing endogenous RNA (ceRNA) network by integrating competing relationships among CETs, miRNAs, lncRNAs and circRNAs were constructed. Furthermore, we constructed a hypoxic adaptation related ceRNA network to identified that 8 miRNAs and 15 circRNAs were predicted to regulated MAPKAPK3, PXN, NFATC2, ATP7A, DIAPH1 and F2R genes. Conclusion: In conclusion, our data reinforce the view that the molecular network of high-altitude adaptation is composed of several protein-coding transcripts and non-coding transcripts that involved in multiply hypoxic adaptation regulatory pathways. The detailed mechanism for how this network crosstalk each other in heart of Bovidae are worthy of future research efforts.

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Comparative analysis of the microRNA transcriptome between yak and cattle provides insight into high-altitude adaptation

Cited by 50 publications

References 52 publications

microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation

microRNA profiling in the Weddell seal suggests novel regulatory mechanisms contributing to diving adaptation

microRNA profiling in the Weddell Seal suggests novel regulatory mechanisms contributing to diving adaptation

Whole-transcriptome analysis of heart in bovidae reveals regulatory pathways associated with high-altitude adaptation

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