Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle

Cold stress is an important factor affecting cattle health, production performance, and reproductive efficiency. Understanding of the potential mechanism underlying genetic adaptation to local environments, particularly extreme cold environment, is limited. Here, by using FLK and hapFLK methods, we...

Full description

Bibliographic Details
Main Authors: Luyu Wang, Yaping Gao, Jinpeng Wang, Ning Huang, Qiang Jiang, Zhihua Ju, Chunhong Yang, Xiaochao Wei, Yao Xiao, Yaran Zhang, Ling Yang, Jinming Huang
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/13/10/1910
_version_ 1797473171522191360
author Luyu Wang
Yaping Gao
Jinpeng Wang
Ning Huang
Qiang Jiang
Zhihua Ju
Chunhong Yang
Xiaochao Wei
Yao Xiao
Yaran Zhang
Ling Yang
Jinming Huang
author_facet Luyu Wang
Yaping Gao
Jinpeng Wang
Ning Huang
Qiang Jiang
Zhihua Ju
Chunhong Yang
Xiaochao Wei
Yao Xiao
Yaran Zhang
Ling Yang
Jinming Huang
author_sort Luyu Wang
collection DOAJ
description Cold stress is an important factor affecting cattle health, production performance, and reproductive efficiency. Understanding of the potential mechanism underlying genetic adaptation to local environments, particularly extreme cold environment, is limited. Here, by using FLK and hapFLK methods, we found that the Zinc finger CCCH-type containing 10 (<i>ZC3H10</i>) gene underwent positive selection in the Menggu, Fuzhou, Anxi, and Shigatse humped cattle breeds that are distributed in the cold areas of China. Furthermore, <i>ZC3H10</i> expression significantly increased in bovine fetal fibroblast (BFF) cells at 28 °C for 4 h. ZC3H10 knockout BFFs were generated using CRISPR/Cas9. Wild and ZC3H10-deleted BFFs were treated at two temperatures and were divided into four groups (WT, wild and cultured at 38 °C; KO, ZC3H10<sup>−/−</sup> and 38 °C; WT_LT, wild, and 28 °C for 4 h; and KO_LT, ZC3H10<sup>−/−</sup> and 28 °C for 4 h. A total of 466, 598, 519, and 650 differently expressed genes (two-fold or more than two-fold changes) were identified by determining transcriptomic difference (KO_LT vs. KO, WT_LT vs. WT, KO vs. WT, and KO_LT vs. WT_LT, respectively). Loss of ZC3H10 dysregulated pathways involved in thermogenesis and immunity, and ZC3H10 participated in immunity-related pathways induced by cold stress and regulated genes involved in glucose and lipid metabolism and lipid transport (PLTP and APOA1), thereby facilitating adaptability to cold stress. Our findings provide a foundation for further studies on the function of ZC3H10 in cold stress and development of bovine breeding strategies for combatting the influences of cold climate.
first_indexed 2024-03-09T20:11:10Z
format Article
id doaj.art-e6abaecf3c424980af2128ac0f979a56
institution Directory Open Access Journal
issn 2073-4425
language English
last_indexed 2024-03-09T20:11:10Z
publishDate 2022-10-01
publisher MDPI AG
record_format Article
series Genes
spelling doaj.art-e6abaecf3c424980af2128ac0f979a562023-11-24T00:17:13ZengMDPI AGGenes2073-44252022-10-011310191010.3390/genes13101910Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native CattleLuyu Wang0Yaping Gao1Jinpeng Wang2Ning Huang3Qiang Jiang4Zhihua Ju5Chunhong Yang6Xiaochao Wei7Yao Xiao8Yaran Zhang9Ling Yang10Jinming Huang11Key Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaDepartment of Animal Science, School of Life Science and Food Engineering, Hebei University of Engineering, Handan 056038, ChinaKey Laboratory of Livestock and Poultry Multi-Omics of MARA, Institute of Animal Science and Veterinary Medicine, Shandong Academy of Agricultural Sciences, Jinan 250100, ChinaCold stress is an important factor affecting cattle health, production performance, and reproductive efficiency. Understanding of the potential mechanism underlying genetic adaptation to local environments, particularly extreme cold environment, is limited. Here, by using FLK and hapFLK methods, we found that the Zinc finger CCCH-type containing 10 (<i>ZC3H10</i>) gene underwent positive selection in the Menggu, Fuzhou, Anxi, and Shigatse humped cattle breeds that are distributed in the cold areas of China. Furthermore, <i>ZC3H10</i> expression significantly increased in bovine fetal fibroblast (BFF) cells at 28 °C for 4 h. ZC3H10 knockout BFFs were generated using CRISPR/Cas9. Wild and ZC3H10-deleted BFFs were treated at two temperatures and were divided into four groups (WT, wild and cultured at 38 °C; KO, ZC3H10<sup>−/−</sup> and 38 °C; WT_LT, wild, and 28 °C for 4 h; and KO_LT, ZC3H10<sup>−/−</sup> and 28 °C for 4 h. A total of 466, 598, 519, and 650 differently expressed genes (two-fold or more than two-fold changes) were identified by determining transcriptomic difference (KO_LT vs. KO, WT_LT vs. WT, KO vs. WT, and KO_LT vs. WT_LT, respectively). Loss of ZC3H10 dysregulated pathways involved in thermogenesis and immunity, and ZC3H10 participated in immunity-related pathways induced by cold stress and regulated genes involved in glucose and lipid metabolism and lipid transport (PLTP and APOA1), thereby facilitating adaptability to cold stress. Our findings provide a foundation for further studies on the function of ZC3H10 in cold stress and development of bovine breeding strategies for combatting the influences of cold climate.https://www.mdpi.com/2073-4425/13/10/1910<i>ZC3H10</i>cold adaptationtranscriptomeCRISPR/Cas9cattle
spellingShingle Luyu Wang
Yaping Gao
Jinpeng Wang
Ning Huang
Qiang Jiang
Zhihua Ju
Chunhong Yang
Xiaochao Wei
Yao Xiao
Yaran Zhang
Ling Yang
Jinming Huang
Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
Genes
<i>ZC3H10</i>
cold adaptation
transcriptome
CRISPR/Cas9
cattle
title Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
title_full Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
title_fullStr Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
title_full_unstemmed Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
title_short Selection Signature and CRISPR/Cas9-Mediated Gene Knockout Analyses Reveal <i>ZC3H10</i> Involved in Cold Adaptation in Chinese Native Cattle
title_sort selection signature and crispr cas9 mediated gene knockout analyses reveal i zc3h10 i involved in cold adaptation in chinese native cattle
topic <i>ZC3H10</i>
cold adaptation
transcriptome
CRISPR/Cas9
cattle
url https://www.mdpi.com/2073-4425/13/10/1910
work_keys_str_mv AT luyuwang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT yapinggao selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT jinpengwang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT ninghuang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT qiangjiang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT zhihuaju selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT chunhongyang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT xiaochaowei selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT yaoxiao selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT yaranzhang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT lingyang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle
AT jinminghuang selectionsignatureandcrisprcas9mediatedgeneknockoutanalysesrevealizc3h10iinvolvedincoldadaptationinchinesenativecattle