Dataset Information

Analysis of Multiplicity of Hypoxia-Inducible Factors in the Evolution of Triplophysa Fish (Osteichthyes: Nemacheilinae) Reveals Hypoxic Environments Adaptation to Tibetan Plateau.

ABSTRACT: HIF (Hypoxia-inducible factor) gene family members function as master regulators of cellular and systemic oxygen homeostasis during changes in oxygen availability. Qinghai-Tibet Plateau is a natural laboratory for for long-term hypoxia and cold adaptation. In this context, T. scleroptera that is restricted to >3500 m high-altitude freshwater rivers was selected as the model to compare with a representative species from the plain, P. dabryanus. We cloned different HIF-? and carried out a phylogenetic analysis from invertebrates to vertebrates for identifying HIF-? genes and analyzing their evolutionary history. Intriguingly, the HIF-? has undergone gene duplications might be due to whole-genome duplication (WGD) events during evolution. PAML analysis indicated that HIF-1?A was subjected to positive selection acted on specific sites in Triplophysa lineages. To investigate the relationship between hypoxia adaptation and the regulation of HIF-? stability by pVHL in plateau and plain fish, a series of experiments were carried out. Comparison the luciferase transcriptional activity and protein levels of HIF-?s and the differing interactions of HIF-?s with pVHL, show clear differences between plateau and plain fish. T. scleroptera pVHL could enhance HIF-? transcriptional activity under hypoxia, and functional validation through pVHL protein mutagenesis showed that these mutations increased the stability of HIF-? and its hetero dimerization affinity to ARNT. Our research shows that missense mutations of pVHL induced evolutionary molecular adaptation in Triplophysa fishes living in high altitude hypoxic environments.

SUBMITTER: Chen J

PROVIDER: S-EPMC7235411 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Analysis of Multiplicity of Hypoxia-Inducible Factors in the Evolution of Triplophysa Fish (Osteichthyes: Nemacheilinae) Reveals Hypoxic Environments Adaptation to Tibetan Plateau.

Chen Juan J Shen Yanjun Y Wang Jing J Ouyang Gang G Kang Jingliang J Lv Wenqi W Yang Liandong L He Shunping S

Frontiers in genetics 20200512

HIF (Hypoxia-inducible factor) gene family members function as master regulators of cellular and systemic oxygen homeostasis during changes in oxygen availability. Qinghai-Tibet Plateau is a natural laboratory for for long-term hypoxia and cold adaptation. In this context, T. scleroptera that is restricted to >3500 m high-altitude freshwater rivers was selected as the model to compare with a representative species from the plain, P. dabryanus. We cloned different HIF-α and carried ...[more]

PMID: 32477402

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Project description:Erythropoietin (EPO) is a glycoprotein hormone that plays a principal regulatory role in erythropoiesis and initiates cell homeostatic responses to environmental challenges. The Qinghai-Tibet Plateau is a natural laboratory for hypoxia adaptation. Gymnocypris dobula is a highly specialized plateau schizothoracine fish that is restricted to?>?4500 m high-altitude freshwater rivers and ponds in the Qinghai-Tibet Plateau. The role of EPO in the adaptation of schizothoracine fish to hypoxia is unknown.The EPO and EPO receptor genes from G. dobula and four other schizothoracine fish from various altitudinal habitats were characterized. Schizothoracine EPOs are predicted to possess 2-3 N-glycosylation (NGS) sites, 4-5 casein kinase II phosphorylation (CK2) sites, 1-2 protein kinase C (PKC) phosphorylation sites, and four conserved cysteine residues within four helical domains, with variations in the numbers of NGS and CK2 sites in G. dobula. PAML analysis indicated a d N/d S value (?)?=?1.112 in the G. dobula lineage, and a few amino acids potentially under lineage-specific positive selection were detected within the G. dobula EPO. Similarly, EPO receptors of the two high-altitude schizothoracines (G. dobula and Ptychobarbus kaznakovi), were found to be statistically on the border of positive selection using the branch-site model (P-value?=?0.096), and some amino acids located in the ligand-binding domain and the fibronectin type III domain were identified as potentially positive selection sites. Tissue EPO expression profiling based on transcriptome sequencing of three schizothoracines (G. dobula, Schizothorax nukiangensis Tsao, and Schizothorax prenanti) showed significant upregulation of EPO expression in the brain and less significantly in the gill of G. dobula. The elevated expression together with the rapid evolution of the EPO gene in G. dobula suggested a possible role for EPO in adaptation to hypoxia. To test this hypothesis, Gd-EPO and Sp-EPO were cloned into an expression vector and transfected into the cultured cell line 293 T. Significantly higher cell viability was observed in cells transfected with Gd-EPO than cells harboring Sp-EPO when challenged by hypoxia.The deduced EPO proteins of the schizothoracine fish contain characteristic structures and important domains similar to EPOs from other taxa. The presence of potentially positive selection sites in both EPO and EPOR in G. dobula suggest possible adaptive evolution in the ligand-receptor binding activity of the EPO signaling cascade in G. dobula. Functional study indicated that the EPO from high-altitude schizothoracine species demonstrated features of hypoxic adaptation by reducing toxic effects or improving cell survival when expressed in cultured cells, providing evidence of molecular adaptation to hypoxic conditions in the Qinghai-Tibet Plateau.

Dataset Information

Analysis of Multiplicity of Hypoxia-Inducible Factors in the Evolution of Triplophysa Fish (Osteichthyes: Nemacheilinae) Reveals Hypoxic Environments Adaptation to Tibetan Plateau.

Publications

Analysis of Multiplicity of Hypoxia-Inducible Factors in the Evolution of <i>Triplophysa</i> Fish (Osteichthyes: Nemacheilinae) Reveals Hypoxic Environments Adaptation to Tibetan Plateau.

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