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Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism.

ABSTRACT: The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.

SUBMITTER: Romanenko SA

PROVIDER: S-EPMC7230192 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism.

Romanenko Svetlana A SA Smorkatcheva Antonina V AV Kovalskaya Yulia M YM Prokopov Dmitry Yu DY Lemskaya Natalya A NA Gladkikh Olga L OL Polikarpov Ivan A IA Serdyukova Natalia A NA Trifonov Vladimir A VA Molodtseva Anna S AS O'Brien Patricia C M PCM Golenishchev Feodor N FN Ferguson-Smith Malcolm A MA Graphodatsky Alexander S AS

Genes 20200330 4

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, mol ...[more]

PMID: 32235544

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Project description:BackgroundSubterranean rodents have evolved many features to adapt to their hypoxic environment. The brain is an organ that is particularly vulnerable to damage caused by exposure to hypoxic conditions. To investigate the mechanisms of adaption to a hypoxic underground environment, we carried out a cross-species brain transcriptome analysis by RNA sequencing and identified genes that are differentially expressed between the subterranean vole Lasiopodomys mandarinus and the closely related above-ground species Lasiopodomys brandtii under chronic hypoxia [10.0% oxygen (O2)] and normoxia (20.9% O2).ResultsA total of 355 million clean reads were obtained, including 69,611 unigenes in L. mandarinus and 69,360 in L. brandtii. A total of 235 and 92 differentially expressed genes (DEGs) were identified by comparing the hypoxic and control groups of L. mandarinus and L. brandtii, respectively. A Gene Ontology (GO) analysis showed that upregulated DEGs in both species had similar functions in response to hypoxia, whereas downregulated DEGs in L. mandarinus were enriched GO terms related to enzymes involved in aerobic reactions. In the Kyoto Encyclopedia of Genes and Genomes pathway analysis, upregulated DEGs in L. mandarinus were associated with angiogenesis and the increased O2 transport capacity of red blood cells, whereas downregulated DEGs were associated with immune responses. On the other hand, upregulated DEGs in L. brandtii were associated with cell survival, vascular endothelial cell proliferation, and neuroprotection, while downregulated genes were related to the synaptic transmission by neurons.ConclusionsL. mandarinus actively adapts its physiological functions to hypoxic conditions, for instance by increasing O2 transport capacity and modulating O2 consumption. In contrast, L. brandtii reacts passively to hypoxia by decreasing overall activity in order to reduce O2 consumption. These results provide insight into hypoxia adaptation mechanisms in subterranean rodents that may be applicable to humans living at high altitudes or operating in other O2-poor environments.

Project description:Background:Severe hypoxia induces a series of stress responses in mammals; however, subterranean rodents have evolved several adaptation mechanisms of energy metabolisms and O2 utilization for hypoxia. Mammalian brains show extreme aerobic metabolism. Following hypoxia exposure, mammals usually experience irreversible brain damage and can even develop serious diseases, such as hypoxic ischemic encephalopathy and brain edema. To investigate mechanisms underlying the responses of subterranean rodents to severe hypoxia, we performed a cross-species brain transcriptomic analysis using RNA sequencing and identified differentially expressed genes (DEGs) between the subterranean rodent Lasiopodomys mandarinus and its closely related aboveground species L. brandtii under severe hypoxia (5.0% O2, 6?h) and normoxia (20.9% O2, 6?h). Results:We obtained 361 million clean reads, including 69,611 unigenes in L. mandarinus and 69,360 in L. brandtii. We identified 359 and 515 DEGs by comparing the hypoxic and normoxia groups of L. mandarinus and L. brandtii, respectively. Gene Ontology (GO) analysis showed that upregulated DEGs in both species displayed similar terms in response to severe hypoxia; the main difference is that GO terms of L. brandtii were enriched in the immune system. However, in the downregulated DEGs, GO terms of L. mandarinus were enriched in cell proliferation and protein transport and those of L. brandtii were enriched in nuclease and hydrolase activities, particularly in terms of developmental functions. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that upregulated DEGs in L. mandarinus were associated with DNA repair and damage prevention as well as angiogenesis and metastasis inhibition, whereas downregulated DEGs were associated with neuronal synaptic transmission and tumor-associated metabolic pathways. In L. brandtii, upregulated KEGG pathways were enriched in the immune, endocrine, and cardiovascular systems and particularly in cancer-related pathways, whereas downregulated DEGs were associated with environmental information processing and misregulation in cancers. Conclusions:L. mandarinus has evolved hypoxia adaptation by enhancing DNA repair, damage prevention, and augmenting sensing, whereas L. brandtii showed a higher risk of tumorigenesis and promoted innate immunity toward severe hypoxia. These results reveal the hypoxic mechanisms of L. mandarinus to severe hypoxia, which may provide research clues for hypoxic diseases.

Dataset Information

Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism.

Publications

Complex Structure of <i>Lasiopodomys mandarinus vinogradovi</i> Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism.

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