Sex-specific gene expression in the blood of four primates

Wang, Jiao; Lan, Yue; He, Lewei; Tang, Ruixiang; Li, Yuhui; Huang, Yuan; Shan, Liang; Gao, Zhan; Price, Megan; Yue, Bisong; He, Miao; Guo, Tao; Fan, Zhenxin

doi:10.1016/j.ygeno.2021.06.007

Cited by 7 publications

(9 citation statements)

References 68 publications

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“…X-degenerate Y-linked genes are those genes that do, or did, have functional copies on both the ancestral X and Y. We found that TXLNGY , for example, had pseudogenized in all studied apes, despite originally being annotated as a functional gene in humans 11 , potentially due to its expression in humans 70 . Similarly, MXRA5Y and PRKY were lost completely in siamang and both orangutans, and pseudogenized in nearly all African apes.…”

Section: Resultsmentioning

confidence: 81%

The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

Makova,

Pickett,

Harris

et al. 2023

Preprint

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Apes possess two sex chromosomes—the male-specific Y and the X shared by males and females. The Y chromosome is crucial for male reproduction, with deletions linked to infertility. The X chromosome carries genes vital for reproduction and cognition. Variation in mating patterns and brain function among great apes suggests corresponding differences in their sex chromosome structure and evolution. However, due to their highly repetitive nature and incomplete reference assemblies, ape sex chromosomes have been challenging to study. Here, using the state-of-the-art experimental and computational methods developed for the telomere-to-telomere (T2T) human genome, we produced gapless, complete assemblies of the X and Y chromosomes for five great apes (chimpanzee, bonobo, gorilla, Bornean and Sumatran orangutans) and a lesser ape, the siamang gibbon. These assemblies completely resolved ampliconic, palindromic, and satellite sequences, including the entire centromeres, allowing us to untangle the intricacies of ape sex chromosome evolution. We found that, compared to the X, ape Y chromosomes vary greatly in size and have low alignability and high levels of structural rearrangements. This divergence on the Y arises from the accumulation of lineage-specific ampliconic regions and palindromes (which are shared more broadly among species on the X) and from the abundance of transposable elements and satellites (which have a lower representation on the X). Our analysis of Y chromosome genes revealed lineage-specific expansions of multi-copy gene families and signatures of purifying selection. In summary, the Y exhibits dynamic evolution, while the X is more stable. Finally, mapping short-read sequencing data from >100 great ape individuals revealed the patterns of diversity and selection on their sex chromosomes, demonstrating the utility of these reference assemblies for studies of great ape evolution. These complete sex chromosome assemblies are expected to further inform conservation genetics of nonhuman apes, all of which are endangered species.

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Section: Resultsmentioning

confidence: 81%

The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

Makova,

Pickett,

Harris

et al. 2023

Preprint

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“…Another group of macaques, sequenced differently from the methylation group, was used for gene expression studies. Raw counts and TPM values of M. thibetana (TM; age: 15-18; male n = 2; female n = 3) and M. mulatta lasiota (CR; age: 15; male n = 3; female n = 3) were obtained from published laboratory studies (Wang et al, 2021).…”

Section: Gene Expression Analysismentioning

confidence: 99%

“…Transcriptome data of M. fascicularis (CE; age: 15-17; male n = 4; female n = 6) were sequenced and analyzed using the same procedures as previous studies (Wang et al, 2021).…”

Section: Gene Expression Analysismentioning

confidence: 99%

DNA methylation and transcriptome analysis reveal epigenomic differences among three macaque species

Wang,

Liu,

Lan

et al. 2023

Evolutionary Applications

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Macaques (genus Macaca) are the most widely distributed non‐human primates, and their evolutionary history, gene expression profiles, and genetic differences have been extensively studied. However, the DNA methylomes of macaque species are not available in public databases, which hampers understanding of epigenetic differences among macaque species. Epigenetic modifications can potentially affect development, physiology, behavior, and evolution. Here, we investigated the methylation patterns of the Tibetan macaque (M. thibetana; TM), Chinese rhesus macaque (M. mulatta lasiota; CR), and crab‐eating macaque (M. fascicularis; CE) through whole‐genome bisulfite sequencing from peripheral blood. We compared genome‐wide methylation site information for the three species. We identified 12,128 (CR vs. CE), 59,165 (CR vs. TM), and 39,751 (CE vs. TM) differentially methylated regions (DMRs) in the three macaques. Furthermore, we obtained the differentially expressed genes (DEGs) among the three macaque species. The differences between CR and CE were smaller at both the methylome and transcriptome levels than compared with TM (CR vs. TM and CE vs. TM). We also found a change in the density of single nucleotide mutations in DMRs relative to their flanking regions, indicating a potential mechanism through which genomic alterations may modulate methylation landscapes, thereby influencing the transcriptome. Functional enrichment analyses showed the DMR‐related genes were enriched in developmental processes and neurological functions, such as the growth hormone‐related pathway, insulin secretion pathway, thyroid hormone synthesis pathway, morphine addiction, and GABAergic synapses. These differences may be associated with variations in physiology and habitat among the macaques. Our study provides one of the first genome‐wide comparisons of genetic, gene expression, and epigenetic variations across different macaques. Our results should facilitate further research on comparative genomic and genetic differences in macaque species.

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“…Sex incompatibility checks. To exclude incorrectly determined sex due to hermaphroditism or morphological misjudgment, six genes located on the Y chromosome (RPS4Y1, RPS4Y2, KDM5D, DDX3Y, USP9Y, and ZFY) and known to be highly expressed in blood tissue of rhesus macaques 34 , were selected as gene markers for sex incompatibility checks. Reads counts for these markers were extracted from all samples, and dimensionality reduction was performed using UMAP 46 in the R package uwot v0.1.14 47 .…”

Section: Transcriptome Data Analysismentioning

confidence: 99%

Unveiling Developmental Trajectory in Infant Macaques: Insights from Longitudinal Multi-omics Studies and Comparative with Humans

Fan,

He,

Lan

et al. 2023

Preprint

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The functional dynamics within the gut microbiota and host of infants remain poorly understood. Here, blood transcriptomes and fecal metagenomes were sequenced from 21 rhesus macaques (Macaca mulatta) infants at seven distinct time points over a 468-day period (6–22 months of age) to trace gene expression patterns and gut microbiota maturation. We found functions of the “core” gut microbial community remained relatively stable, but there were fluctuations in the composition and abundance of gut microbiota. Alterations in the fecal metagenome were correlated with changes in diet and environment, while shifts in the blood transcriptome were indicative of developmental and immunological trends. The overall trend of the gut microbiota of both humans and macaques to reach adult-like configurations was comparable, albeit with notable differences in developmental trajectories. Our study emphasizes the potential utility of infant macaques as suitable models for human infant development, particularly with respect to gut microbial maturation.

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Sex-specific gene expression in the blood of four primates

Cited by 7 publications

References 68 publications

The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

The Complete Sequence and Comparative Analysis of Ape Sex Chromosomes

DNA methylation and transcriptome analysis reveal epigenomic differences among three macaque species

Unveiling Developmental Trajectory in Infant Macaques: Insights from Longitudinal Multi-omics Studies and Comparative with Humans

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