Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats

The Zhongwei goat is kept primarily for its beautiful white, curly pelt that appears when the kid is approximately 1 month old; however, this representative phenotype often changes to a less curly phenotype during postnatal development in a process that may be mediated by multiple molecular signals....

Full description

Bibliographic Details
Main Authors: Ping Xiao, Tao Zhong, Zhanfa Liu, Yangyang Ding, Weijun Guan, Xiaohong He, Yabin Pu, Lin Jiang, Yuehui Ma, Qianjun Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-01-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2019.01263/full
_version_ 1818322318010613760
author Ping Xiao
Ping Xiao
Tao Zhong
Zhanfa Liu
Yangyang Ding
Weijun Guan
Xiaohong He
Yabin Pu
Lin Jiang
Yuehui Ma
Qianjun Zhao
author_facet Ping Xiao
Ping Xiao
Tao Zhong
Zhanfa Liu
Yangyang Ding
Weijun Guan
Xiaohong He
Yabin Pu
Lin Jiang
Yuehui Ma
Qianjun Zhao
author_sort Ping Xiao
collection DOAJ
description The Zhongwei goat is kept primarily for its beautiful white, curly pelt that appears when the kid is approximately 1 month old; however, this representative phenotype often changes to a less curly phenotype during postnatal development in a process that may be mediated by multiple molecular signals. DNA methylation plays important roles in mammalian cellular processes and is essential for the initiation of hair follicle (HF) development. Here, we sought to investigate the effects of genome-wide DNA methylation by combining expression profiles of the underlying curly fleece dynamics. Genome-wide DNA methylation maps and transcriptomes of skin tissues collected from 45- to 108-day-old goats were used for whole-genome bisulfite sequencing (WGBS) and RNA sequencing, respectively. Between the two developmental stages, 1,250 of 3,379 differentially methylated regions (DMRs) were annotated in differentially methylated genes (DMGs), and these regions were mainly related to intercellular communication and the cytoskeleton. Integrated analysis of the methylome and transcriptome data led to the identification of 14 overlapping genes that encode crucial factors for wool fiber development through epigenetic mechanisms. Furthermore, a functional study using human hair inner root sheath cells (HHIRSCs) revealed that, one of the overlapping genes, platelet-derived growth factor C (PDGFC) had a significant effect on the messenger RNA expression of several key HF-related genes that promote cell migration and proliferation. Our study presents an unprecedented analysis that was used to explore the enigma of fleece morphological changes by combining methylome maps and transcriptional expression, and these data revealed stage-specific epigenetic changes that potentially affect fiber development. Furthermore, our functional study highlights a possible role for the overlapping gene PDGFC in HF cell growth, which may be a predictable biomarker for fur goat selection.
first_indexed 2024-12-13T10:54:53Z
format Article
id doaj.art-4e2fc1cfd912439cacbd2d1695737b7d
institution Directory Open Access Journal
issn 1664-8021
language English
last_indexed 2024-12-13T10:54:53Z
publishDate 2020-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Genetics
spelling doaj.art-4e2fc1cfd912439cacbd2d1695737b7d2022-12-21T23:49:37ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-01-011010.3389/fgene.2019.01263455388Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei GoatsPing Xiao0Ping Xiao1Tao Zhong2Zhanfa Liu3Yangyang Ding4Weijun Guan5Xiaohong He6Yabin Pu7Lin Jiang8Yuehui Ma9Qianjun Zhao10Key Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaFarm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, ChinaFarm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu, ChinaThe Ningxia Hui Autonomous Region Breeding Ground of Zhongwei Goat, Department of Agriculture and Rural Areas of Ningxia Hui Autonomous Region, Wuzhong, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaKey Laboratory of Animal (Poultry) Genetics Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing, ChinaThe Zhongwei goat is kept primarily for its beautiful white, curly pelt that appears when the kid is approximately 1 month old; however, this representative phenotype often changes to a less curly phenotype during postnatal development in a process that may be mediated by multiple molecular signals. DNA methylation plays important roles in mammalian cellular processes and is essential for the initiation of hair follicle (HF) development. Here, we sought to investigate the effects of genome-wide DNA methylation by combining expression profiles of the underlying curly fleece dynamics. Genome-wide DNA methylation maps and transcriptomes of skin tissues collected from 45- to 108-day-old goats were used for whole-genome bisulfite sequencing (WGBS) and RNA sequencing, respectively. Between the two developmental stages, 1,250 of 3,379 differentially methylated regions (DMRs) were annotated in differentially methylated genes (DMGs), and these regions were mainly related to intercellular communication and the cytoskeleton. Integrated analysis of the methylome and transcriptome data led to the identification of 14 overlapping genes that encode crucial factors for wool fiber development through epigenetic mechanisms. Furthermore, a functional study using human hair inner root sheath cells (HHIRSCs) revealed that, one of the overlapping genes, platelet-derived growth factor C (PDGFC) had a significant effect on the messenger RNA expression of several key HF-related genes that promote cell migration and proliferation. Our study presents an unprecedented analysis that was used to explore the enigma of fleece morphological changes by combining methylome maps and transcriptional expression, and these data revealed stage-specific epigenetic changes that potentially affect fiber development. Furthermore, our functional study highlights a possible role for the overlapping gene PDGFC in HF cell growth, which may be a predictable biomarker for fur goat selection.https://www.frontiersin.org/article/10.3389/fgene.2019.01263/fullZhongwei goatdeoxyribonucleic acid methylationcurly peltsepigeneticstranscriptomicsplatelet-derived growth factor C
spellingShingle Ping Xiao
Ping Xiao
Tao Zhong
Zhanfa Liu
Yangyang Ding
Weijun Guan
Xiaohong He
Yabin Pu
Lin Jiang
Yuehui Ma
Qianjun Zhao
Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
Frontiers in Genetics
Zhongwei goat
deoxyribonucleic acid methylation
curly pelts
epigenetics
transcriptomics
platelet-derived growth factor C
title Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
title_full Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
title_fullStr Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
title_full_unstemmed Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
title_short Integrated Analysis of Methylome and Transcriptome Changes Reveals the Underlying Regulatory Signatures Driving Curly Wool Transformation in Chinese Zhongwei Goats
title_sort integrated analysis of methylome and transcriptome changes reveals the underlying regulatory signatures driving curly wool transformation in chinese zhongwei goats
topic Zhongwei goat
deoxyribonucleic acid methylation
curly pelts
epigenetics
transcriptomics
platelet-derived growth factor C
url https://www.frontiersin.org/article/10.3389/fgene.2019.01263/full
work_keys_str_mv AT pingxiao integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT pingxiao integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT taozhong integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT zhanfaliu integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT yangyangding integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT weijunguan integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT xiaohonghe integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT yabinpu integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT linjiang integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT yuehuima integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats
AT qianjunzhao integratedanalysisofmethylomeandtranscriptomechangesrevealstheunderlyingregulatorysignaturesdrivingcurlywooltransformationinchinesezhongweigoats