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Journal of Integrative Agriculture  2022, Vol. 21 Issue (11): 3293-3301    DOI: 10.1016/j.jia.2022.08.061
Special Issue: 动物科学Animal Science
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |

Genome-wide detection for runs of homozygosity analysis in three pig breeds from Chinese Taihu Basin and Landrace pigs by SLAF-seq data

TONG Shi-feng1, 2, ZHU Mo1, 2, XIE Rui1, LI Dong-feng1, ZHANG Li-fan1, LIU Yang1, 2

1 Department of Animal Genetics, Breeding and Reproduction, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 Key Laboratory of Urban Agriculture, Ministry of Agriculture and Rural Affairs, Shanghai 200240, P.R.China


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摘要  

二花脸猪、梅山猪和米猪是我国太湖流域优良的地方猪品种,为商品猪的遗传改良做出了巨大贡献。分析这3个猪种的遗传结构和近交水平,对地方猪遗传多样性的保护以及商品猪的持续改良具有重要意义。长纯合片段(Runs of homozygosityROH)的长度、数量以及在基因组中的分布模式可以作为评价群体近交水平和物种起源的指标。本研究利用SLAF-seq数据对4个不同品种(二花脸猪、梅山猪、米猪和长白猪)的猪群体进行全基因组ROH 检测,并根据ROH信息计算了各个猪群体的近交系数(FROH)。此外,研究还在高频ROH区域筛选与母猪繁殖性状相关的候选基因。在4个猪种的116个个体中共检测到10,568ROHPCA分析表明,太湖流域3个猪种的遗传结构与长白猪存在显著差异,而二花脸猪和米猪的遗传结构较为相似。4个猪群体中,长白猪短ROH(<5 Mb的频率最高,而梅山猪长ROH>5 Mb)的频率最高,明显高于二花脸猪和米猪。梅山猪个体ROH覆盖总基因组的长度和ROH总数接近于长白猪,也明显高于二花脸猪和米猪。同时,梅山猪的平均FROH最高与长白猪相近,二花脸猪的平均FROH最低与米猪相近。以上结果表明梅山猪和长白猪一样表现出较高的近交水平,梅山猪较高的近交水平主要来源于近代的近亲繁殖,而二花脸猪和米猪的近交水平相对较低。此外,大量与母猪繁殖性状相关的候选基因在高频ROH区被鉴定到,这些基因有望作为标记辅助选择(MAS)育种的候选基因。本研究的结果为太湖流域3个猪种的遗传多样性保护、防止近交衰退和遗传改良提供了理论依据。



Abstract  


Erhualian (E), Meishan (MS) and Mi (MI) pigs are excellent indigenous pig breeds in Chinese Taihu Basin, which have made great contributions to the genetic improvement of commercial pigs.  Investigation of the genetic structure and inbreeding level of the 3 pig breeds is of great significance for the sustainable breeding of commercial pigs.  The length and number of runs of homozygosity (ROH) as well as the frequency of genomes covered by ROH can be used as indicators to evaluate the level of inbreeding and the origin of the population.  In this study, the ROH characteristics of E, MS, MI and Landrace (L) pigs were analyzed by SLAF-seq data, and the inbreeding coefficient based on ROH (FROH) was calculated.  In addition, we have identified candidate genes in the genomic regions associated with ROH.  A total of 10 568 ROH were detected in 116 individuals of 4 pig breeds.  The analysis showed that there were significant differences in genetic structure between 3 Taihu Basin pig breeds and L, and the genetic structure of E and MI was similar.  The results of FROH showed that the inbreeding level of MS was the highest (0.25±0.07), while E and MI were lower than L.  Compared with the other 3 pig populations, MS showed a higher frequency of long ROH (>5 Mb), indicating higher inbreeding in MS in recent generations.  A large number of candidate genes related to reproductive traits are located in the genomic regions with a high frequency of ROH, and these genes are expected to be used as candidate genes in marker-assisted selection (MAS) breeding programs.  Our findings can provide theoretical support for genetic conservation and genetic improvement of 3 pig breeds in Chinese Taihu Basin.



Keywords:  runs of homozygosity       inbreeding coefficient       pig       candidate gene  
Received: 04 September 2021   Accepted: 28 April 2022
Fund: 

This research was supported by the Jiangsu Agricultural Science and Technology Innovation Found, China (SCX (20) 3290), the Open Foundation of Key Laboratory of Urban Agriculture, Ministry of Agriculture and Rural Affairs of China (201906), and the Joint Research Project on Pig Breeding in Anhui Province, China (340000211260001000431).

About author:  TONG Shi-feng, Tel: +86-15764383842, E-mail: sftong9518@163.com; Correspondence LIU Yang, Tel: +86-25-84395346, E-mail: yangliu@naju.edu.cn *These authors contributed equally to this study

Cite this article: 

TONG Shi-feng, ZHU Mo , XIE Rui , LI Dong-feng , ZHANG Li-fan , LIU Yang. 2022.

Genome-wide detection for runs of homozygosity analysis in three pig breeds from Chinese Taihu Basin and Landrace pigs by SLAF-seq data . Journal of Integrative Agriculture, 21(11): 3293-3301.

Bosse M, Megens H J, Frantz L A F, Madsen O, Larson G, Paudel Y, Duijvesteijn N, Harlizius B, Hagemeijer Y, Crooijmans R P M A, Groenen M A M. 2014. Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nature Communications, 5, 4392.
Bosse M, Megens H J, Madsen O, Paudel Y, Frantz L A F, Schook L B, Crooijmans R P M A, Groenen M A M. 2012. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genetics, 8, e1003100.
Brito L F, Kijas J W, Ventura R V, Sargolzaei M, Porto-Neto L R, Cánovas A, Feng Z, Jafarikia M, Schenkel F S. 2017. Genetic diversity and signatures of selection in various goat breeds revealed by genome-wide SNP markers. BMC Genomics, 18, 229.
Cassará M C, Menzel V A, Hinsch K D, Wrenzycki C, Hinsch E. 2009. Voltage-dependent anion channels 1 and 2 are expressed in porcine oocytes. Bioscience Reports, 30, 193–200.
Ceballos F C, Joshi P K, Clark D W, Ramsay M, Wilson J F. 2018. Runs of homozygosity: Windows into population history and trait architecture. Nature Reviews Genetics, 19, 220–234.
Dai Y, Newman B, Moor R. 2005. Translational regulation of MOS messenger RNA in pig oocytes. Biology of Reproduction, 73, 997–1003.
Fang X, Ji H, Kim S W, Park J I, Vaught T G, Anastasiadis P Z, Ciesiolka M, McCrea P D. 2004. Vertebrate development requires ARVCF and p120 catenins and their interplay with RhoA and Rac. The Journal of Cell Biology, 165, 87–98.
Firat-Karalar E N, Sante J, Elliott S, Stearns T. 2014. Proteomic analysis of mammalian sperm cells identifies new components of the centrosome. Journal of Cell Science, 127, 4128–4133.
Hassoun R, Schwartz P, Feistel K, Blum M, Viebahn C. 2009. Axial differentiation and early gastrulation stages of the pig embryo. Differentiation Research in Biological Diversity, 78, 301–311.
Karpeta A, Warzecha K, Jerzak J, Ptak A, Gregoraszczuk E L. 2012. Activation of the enzymes of phase I (CYP2B1/2) and phase II (SULT1A and COMT) metabolism by 2,2´,4,4´-tetrabromodiphenyl ether (BDE47) in the pig ovary. Reproductive Toxicology, 34, 436–442.
Kobayashi T, Zhang H, Tang W W C, Irie N, Withey S, Klisch D, Sybirna A, Dietmann S, Contreras D A, Webb R, Allegrucci C, Alberio R, Surani M A. 2017. Principles of early human development and germ cell program from conserved model systems. Nature, 546, 416–420.
Lencz T, Lambert C, DeRosse P, Burdick K E, Morgan T V, Kane J M, Kucherlapati R, Malhotra A K. 2007. Runs of homozygosity reveal highly penetrant recessive loci in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America, 104, 19942–19947.
Li F, Han H, Lei Q, Gao J, Liu J, Liu W, Zhou Y, Li H, Cao D. 2018. Genome-wide association study of body weight in Wenshang Barred chicken based on the SLAF-seq technology. Journal of Applied Genetics, 59, 305–312.
Li Y, Pu L, Shi L, Gao H, Zhang P, Wang L, Zhao F. 2021. Revealing new candidate genes for teat number relevant traits in Duroc pigs using genome-wide association studies. Animals, 11, 806.
Li Z, Wei S, Li H, Wu K, Cai Z, Li D, Wei W, Li Q, Chen J, Liu H, Zhang L. 2017. Genome-wide genetic structure and differentially selected regions among Landrace, Erhualian, and Meishan pigs using specific-locus amplified fragment sequencing. Scientific Reports, 7, 10063.
Lin C J, Koh F M, Wong P, Conti M, Ramalho-Santos M. 2014. Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Developmental Cell, 30, 268–279.
Liu J, Shi L, Li Y, Chen L, Garrick D, Wang L, Zhao F. 2021. Estimates of genomic inbreeding and identification of candidate regions that differ between Chinese indigenous sheep breeds. Journal of Animal Science and Biotechnology, 12, 95.
Liu W, Zhao Q, Piao S, Wang C, Kong Q, An T. 2017. Endo-siRNA deficiency results in oocyte maturation failure and apoptosis in porcine oocytes. Reproduction, Fertility, and Development, 29, 2168–2174.
Martinez C A, Cambra J M, Gil M A, Parrilla I, Alvarez-Rodriguez M, Rodriguez-Martinez H, Cuello C, Martinez E A. 2020. Seminal plasma induces overexpression of genes associated with embryo development and implantation in day-6 porcine blastocysts. International Journal of Molecular Sciences, 21, 3662.
Mastrangelo S, Tolone M, Sardina M T, Sottile G, Sutera A M, Di Gerlando R, Portolano B. 2017. Genome-wide scan for runs of homozygosity identifies potential candidate genes associated with local adaptation in Valle del Belice sheep. Genetics Selection Evolution, 49, 84.
Nautiyal J, Kumar P G, Laloraya M. 2004. 17Beta-estradiol induces nuclear translocation of CrkL at the window of embryo implantation. Biochemical and Biophysical Research Communications, 318, 103–112.
Paradis F, Novak S, Murdoch G K, Dyck M K, Dixon W T, Foxcroft G R. 2009. Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction, 138, 115–129.
Paulesu L, Cateni C, Romagnoli R, Ietta F, Dantzer V. 2005. Variation in macrophage-migration-inhibitory-factor immunoreactivity during porcine gestation. Biology of Reproduction, 72, 949–953.
Peripolli E, Munari D P, Silva M V G B, Lima A L F, Irgang R, Baldi F. 2017. Runs of homozygosity: Current knowledge and applications in livestock. Animal Genetics, 48, 255–271.
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M A R, Bender D, Maller J, Sklar P, de Bakker P I W, Daly M J, Sham P C. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559–575.
Sakakura M, Ohta S, Yagi M, Tanaka A, Norihide J, Woltjen K, Yamamoto T, Yamada Y. 2019. Smarcb1 maintains the cellular identity and the chromatin landscapes of mouse embryonic stem cells. Biochemical and Biophysical Research Communications, 519, 705–713.
Schiavo G, Bovo S, Muñoz M, Ribani A, Alves E, Araújo J P, Bozzi R, Čandek-Potokar M, Charneca R, Fernandez A I, Gallo M, García F, Karolyi D, Kušec G, Martins J M, Mercat M J, Núñez Y, Quintanilla R, Radović Č, Razmaite V, et al. 2021. Runs of homozygosity provide a genome landscape picture of inbreeding and genetic history of European autochthonous and commercial pig breeds. Animal Genetics, 52, 155–170.
Shi L, Wang L, Liu J, Deng T, Yan H, Zhang L, Liu X, Gao H, Hou X, Wang L, Zhao F. 2020. Estimation of inbreeding and identification of regions under heavy selection based on runs of homozygosity in a Large White pig population. Journal of Animal Science and Biotechnology, 11, 46.
Shukla V, Kaushal J B, Sankhwar P, Manohar M, Dwivedi A. 2019. Inhibition of TPPP3 attenuates β-catenin/NF-κB/COX-2 signaling in endometrial stromal cells and impairs decidualization. The Journal of Endocrinology, 240, 417–429.
Sun X, Liu D, Zhang X, Li W, Liu H, Hong W, Jiang C, Guan N, Ma C, Zeng H, Xu C, Song J, Huang L, Wang C, Shi J, Wang R, Zheng X, Lu C, Wang X, Zheng H. 2013. SLAF-seq: an efficient method of large-scale de novo SNP discovery and genotyping using high-throughput sequencing. PLoS One, 8, e58700.
Wang L, Sørensen P, Janss L, Ostersen T, Edwards D. 2013. Genome-wide and local pattern of linkage disequilibrium and persistence of phase for 3 Danish pig breeds. BMC Genetics, 14, 115.
Wang S, Li J, Zhang A, Liu M, Zhang H. 2011. Selection of reference genes for studies of porcine endometrial gene expression on gestational day 12. Biochemical and Biophysical Research Communications, 408, 265–268.
Wang X, Wang C, Huang M, Tang J, Fan Y, Li Y, Li X, Ji H, Ren J, Ding N. 2018. Genetic diversity, population structure and phylogenetic relationships of three indigenous pig breeds from Jiangxi Province, China, in a worldwide panel of pigs. Animal Genetics, 49, 275–283.
Wang Z, Chen Q, Yang Y, Liao R, Zhao J, Zhang Z, Chen Z, Zhang X, Xue M, Yang H, Zheng Y, Wang Q, Pan Y. 2015. Genetic diversity and population structure of six Chinese indigenous pig breeds in the Taihu Lake region revealed by sequencing data. Animal Genetics, 46, 697–701.
Wu X, Hu F, Zeng J, Han L, Qiu D, Wang H, Ge J, Ying X, Wang Q. 2019. NMNAT2-mediated NAD+ generation is essential for quality control of aged oocytes. Aging Cell, 18, e12955.
Xia X, Yan C, Wu W, Zhou Y, Hou L, Zuo B, Xu D, Ren Z, Xiong Y. 2016. Characterization of the porcine peptidylarginine deiminase type VI gene (PADI6) promoter: Sp1 regulates basal transcription of the porcine PADI6. Gene, 575, 551–558.
Xie R, Shi L, Liu J, Deng T, Wang L, Liu Y, Zhao F. 2019. Genome-wide scan for runs of homozygosity identifies candidate genes in three pig breeds. Animals, 9, 51.
Zhang S, Li B, Chen Y, Shaibu A S, Zheng H, Sun J. 2020. Molecular-assisted distinctness and uniformity testing using SLAF-sequencing approach in soybean. Genes, 11, 175.
Zhang Z, Zhang Q, Xiao Q, Sun H, Gao H, Yang Y, Chen J, Li Z, Xue M, Ma P, Yang H, Xu N, Wang Q, Pan Y. 2018. Distribution of runs of homozygosity in Chinese and Western pig breeds evaluated by reduced-representation sequencing data. Animal Genetics, 49, 579–591.
Zhao X, Yu Y T. 2004. Pseudouridines in and near the branch site recognition region of U2 snRNA are required for snRNP biogenesis and pre-mRNA splicing in xenopus oocytes. RNA, 10, 681–690.

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