Please wait a minute...
Journal of Integrative Agriculture  2015, Vol. 14 Issue (10): 2027-2033    DOI: 10.1016/S2095-3119(15)61084-X
Animal Science · Veterinary Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Quantitative trait loci for the number of vertebrae on Sus scrofa chromosomes 1 and 7 independently influence the numbers of thoracic and lumbar vertebrae in pigs
 ZHANG Long-chao, LIU Xin, LIANG Jing, YAN Hua, ZHAO Ke-bin, LI Na, PU Lei, SHI Hui-bi, ZHANG Yue-bo, WANG Li-gang, WANG Li-xian
Key Laboratory of Farm Animal Genetic Resources and Germplasm Innovation, Ministry of Agriculture/Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China Abstract
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  Although quantitative trait loci (QTLs) for number of thoracic-lumbar vertebrae have been identified on Sus scrofa chromosomes (SSCs) 1 and 7, the influence of these QTLs on the thoracic and lumbar vertebrae is not clear. The aim of this study was to identify single nucleotide polymorphisms (SNPs) associated with total number of thoracic-lumbar vertebrae and for each trait (number of thoracic and lumbar vertebrae) separately. A total of 581 individuals from an F2 Large White×Minzhu population were genotyped using an SNP60K chip. Performing a genome-wide association study (GWAS) for total number of thoracic-lumbar vertebrae, 38 significant SNPs were identified in two QTL regions located on SSC1 and SSC7. Performing a GWAS for number of thoracic vertebrae only, 72 significant SNPs were located on SSC7. While performing a GWAS for number of lumbar vertebrae only, 17 significant SNPs were identified on SSC1. Gene mining suggested that the gene encoding orphan nuclear receptor, germ cell nuclear factor (NR6A1) on SSC1 was a strong candidate affecting the number of lumbar vertebrae in pigs. Additionally, genes encoding vertnin (VRTN), prospero homeobox 2 (PROX2), Finkel-Biskis-Jinkins murine osteosarcoma viral oncogene homolog (FOS), and transforming growth factor beta 3 (TGFB3) may be important candidates affecting the number of thoracic vertebrae in pigs. QTLs on SSC1 and SSC7 independently influenced the numbers of thoracic and lumbar vertebrae. These results shed light on the complex genetic background of vertebrae development in pigs.

Abstract  Although quantitative trait loci (QTLs) for number of thoracic-lumbar vertebrae have been identified on Sus scrofa chromosomes (SSCs) 1 and 7, the influence of these QTLs on the thoracic and lumbar vertebrae is not clear. The aim of this study was to identify single nucleotide polymorphisms (SNPs) associated with total number of thoracic-lumbar vertebrae and for each trait (number of thoracic and lumbar vertebrae) separately. A total of 581 individuals from an F2 Large White×Minzhu population were genotyped using an SNP60K chip. Performing a genome-wide association study (GWAS) for total number of thoracic-lumbar vertebrae, 38 significant SNPs were identified in two QTL regions located on SSC1 and SSC7. Performing a GWAS for number of thoracic vertebrae only, 72 significant SNPs were located on SSC7. While performing a GWAS for number of lumbar vertebrae only, 17 significant SNPs were identified on SSC1. Gene mining suggested that the gene encoding orphan nuclear receptor, germ cell nuclear factor (NR6A1) on SSC1 was a strong candidate affecting the number of lumbar vertebrae in pigs. Additionally, genes encoding vertnin (VRTN), prospero homeobox 2 (PROX2), Finkel-Biskis-Jinkins murine osteosarcoma viral oncogene homolog (FOS), and transforming growth factor beta 3 (TGFB3) may be important candidates affecting the number of thoracic vertebrae in pigs. QTLs on SSC1 and SSC7 independently influenced the numbers of thoracic and lumbar vertebrae. These results shed light on the complex genetic background of vertebrae development in pigs.
Keywords:  candidate gene       genetic variant       genome-wide association study       number of vertebrae       pig       QTLs  
Received: 31 March 2015   Accepted:
Fund: 

This research was supported by the Agricultural Science and Technology Innovation Program, China (ASTIP-IAS02), the National Key Technology R&D Program of China (2011BAD28B01), the National Natural Science Foundation of China (31201781), the Earmarked Fund for Modern Agro-Industry Technology Research System, the National Key Technology R&D Program of China (2011ZX08006-003) and the Chinese Academy of Agricultural Sciences Foundation (2014ZL006, 2011cj-5, 2012ZL069 and 2014ywf-yb-8).

Corresponding Authors:  WANG Li-xian, Tel: +86-10-62818771,E-mail: iaswlx@263.net; WANG Li-gang, Tel: +86-10-62816011,E-mail: ligwang@126.com   
About author:  Zhang Long-chao, Tel: +86-10-62816011, E-mail: zhlchias@163.com; LIU Xin, Tel: +86-10-62816011, E-mail: firstliuxin@163.com;* These authors contributed equally to this study.

Cite this article: 

ZHANG Long-chao, LIU Xin, LIANG Jing, YAN Hua, ZHAO Ke-bin, LI Na, PU Lei, SHI Hui-bi, ZHANG Yue-bo, WANG Li-gang, WANG Li-xian. 2015. Quantitative trait loci for the number of vertebrae on Sus scrofa chromosomes 1 and 7 independently influence the numbers of thoracic and lumbar vertebrae in pigs. Journal of Integrative Agriculture, 14(10): 2027-2033.

Andersson O, Reissmann E, Ibáñez C F. 2006. Growthdifferentiation factor 11 signals through the transforminggrowth factor-beta receptor ALK5 to regionalize the anteriorposterioraxis. Embo Reports, 7, 831-837

Amin N, van Duijn C M, Aulchenko Y S. 2007. A genomicbackground based method for association analysis inrelated individuals. PLoS One, 2, e1274.

Aulchenko Y S, de Koning D J, Haley C. 2007. Genome-widerapid association using mixed model and regression: Afast and simple method for genome-wide pedigree-basedquantitative trait loci association analysis. Genetics, 177,577-585

Berge S. 1948. Genetical researches on the number ofvertebrae in the pig. Journal of Animal Science, 7, 233-238

Burgos C, Latorre P, Altarriba J, Carrodeguas J A, Varona L,López-Buesa P. 2014. Allelic frequencies of NR6A1 andVRTN, two genes that affect vertebrae number in diversepig breeds: A study of the effects of the VRTN insertion onphenotypic traits of a Duroc×Landrace-Large White cross.Meat Science, 100, 150-155

Cheah F S, Jabs EW, Chong S S. 2005. Genomic, cDNA, andembryonic expression analysis of zebrafish transforminggrowth factor beta 3 (tgf beta3). Developmental Dynamics,232, 1021-1030

Christ B, Huang R, Wilting J. 2000. The development of theavian vertebral column. Anatomy and Embryology (Berl),202, 179-194

Fan Y, Xing Y, Zhang Z, Ai H, Ouyang Z, Ouyang J, Yang M,Li P, Chen Y, Gao J, Li L, Huang L, Ren J. 2013. A further look at porcine chromosome 7 reveals VRTN variantsassociated with vertebral number in Chinese and Westernpigs. PLoS One, 8, e62534.

Fontanesi L, Ribani A, Scotti E, Utzeri V J, Veli?kovi? N, Dall’OlioS. 2014. Differentiation of meat from European wild boarsand domestic pigs using polymorphisms in the MC1R andNR6A1 genes. Meat Science, 98, 781-784

Galis F. 1999. Why do almost all mammals have seven cervicalvertebrae? Developmental constraints, Hox genes, andcancer. Journal of Experimental Zoology, 285, 19-26

King J W B, Roberts R C. 1960. Carcass length in the baconpig: Its association with vertebrae numbers and predictionfrom radiographs of the young pig. Animal ProductionScience, 2, 59-65

Lee Y J, McPherron A, Choe S, Sakai Y, Chandraratna R A, LeeS J, Oh S P. 2010. Growth differentiation factor 11 signalingcontrols retinoic acid activity for axial vertebral development.Developmental Biology, 347, 195-203

Madsen P, Sorensen P, Su G, Damgaard L H, ThomsenH, Labouriau R. 2006. DMU - a package for analyzingmultivariate mixed models. In: Proceedings of the 8th WorldCongress on Genetics Applied to Livestock Production. 13-18 August, 2006. Belo Horizonte, MG, Brazil.

McPherron A C, Lawler A M, Lee S J. 1999. Regulation ofanterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nature Genetics, 22, 260-264

Mikawa S, Hayashi T, Nii M, Shimanuki S, Morozumi T, Awata T.2005. Two quantitative trait loci on Sus scrofa chromosomes1 and 7 affecting the number of vertebrae. Journal of AnimalScience, 83, 2247-2254

Mikawa S, Morozumi T, Shimanuki S, Hayashi T, Uenishi H,Domukai M, Okumura N, Awata T. 2007. Fine mapping ofa swine quantitative trait locus for number of vertebrae andanalysis of an orphan nuclear receptor, germ cell nuclearfactor (NR6A1). Genome Research, 17, 586-593

Mikawa S, Sato S, Nii M, Morozumi T, Yoshioka G, Imaeda N,Yamaguchi T, Hayashi T, Awata T. 2011. Identification of asecond gene associated with variation in vertebral numberin domestic pigs. BMC Genetics, 12, 5.

Miller S A, Dykes D D, Polesky H F. 1988. A simple salting outprocedure for extracting DNA from human nucleated cells.Nucleic Acids Research, 16, 1215.

Ren D R, Ren J, Ruan G F, Guo Y M, Wu L H, Yang G C, ZhouL H, Li L, Zhang Z Y, Huang L S. 2012. Mapping and finemapping of quantitative trait loci for the number of vertebraein a White Duroc×Chinese Erhualian intercross resourcepopulation. Animal Genetics, 43, 545-551

Wada Y, Akita T, Awata T, Furukawa T, Sugai N, Inage Y, IshiiK, Ito Y, Kobayashi E, Kusumoto H, Matsumoto T, MikawaS, Miyake M, Murase A, Shimanuki S, Sugiyama T, UchidaY, Yanai S, Yasue H. 2000. Quantitative trait loci (QTL)analysis in a Meishan×Göttingen cross population. AnimalGenetics, 31, 376-384

Yang G, Ren J, Zhang Z, Huang L. 2009. Genetic evidence forthe introgression of Western NR6A1 haplotype into ChineseLicha breed associated with increased vertebral number.Animal Genetics, 40, 247-250

Zhang L, Liang J, Luo W, Liu X, Yan H, Zhao K, Shi H, ZhangY, Wang L, Wang L. 2014. Genome-wide scan revealsLEMD3 and WIF1 on SSC5 as the candidates for porcineear size. PLoS One, 9, e102085.

Zhang Z G, Li B D, Chen X H. 1986. Pig Breeds in China.Shanghai Scientific and Technical Publisher, China. (inChinese)

Zhao S F, Chai M Z, Wu M, He Y H, Meng T, Shi B.2014. Effect of vitamin B12 on cleft palate induced by2,3,7,8-tetrachlorodibenzo-p-dioxin and dexamethasonein mice. Journal of Zhejiang University Science (B), 15,289-294
[1] Tiantian Chen, Lei Li, Dan Liu, Yubing Tian, Lingli Li, Jianqi Zeng, Awais Rasheed, Shuanghe Cao, Xianchun Xia, Zhonghu He, Jindong Liu, Yong Zhang. Genome wide linkage mapping for black point resistance in a recombinant inbred line population of Zhongmai 578 and Jimai 22[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3311-3321.
[2] Chenyang Wang, Yinuo Zhang, Qiming Sun, Lin Li, Fang Guan, Yazhou He, Yidong Wu. Species-specific evolution of lepidopteran TspC5 tetraspanins associated with dominant resistance to Bacillus thuringiensis toxin Cry1Ac[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3127-3140.
[3] Tengteng Xu, Mengya Zhang, Qiuchen Liu, Xin Wang, Pengfei Luo, Tong Liu, Yelian Yan, Naru Zhou, Yangyang Ma, Tong Yu, Yunsheng Li, Zubing Cao, Yunhai Zhang. 18S ribosomal RNA methyltransferase METTL5-mediated CDX2 translation regulates porcine early embryo development[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3185-3198.
[4] Dan Lü, Jianxin Li, Xuehai Zhang, Ran Zheng, Aoni Zhang, Jingyun Luo, Bo Tong, Hongbing Luo, Jianbing Yan, Min Deng. Genetic analysis of maize crude fat content by multi-locus genome-wide association study[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2475-2491.
[5] Jianqi Zeng, Dehui Zhao, Li Yang, Yufeng Yang, Dan Liu, Yubing Tian, Fengju Wang, Shuanghe Cao, Xianchun Xia, Zhonghu He, Yong Zhang. Fine mapping and candidate gene analysis of a major QTL for grain length on chromosome 5BS in bread wheat[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2465-2474.
[6] Shengzhong Zhang, Xiaohui Hu, Feifei Wang, Huarong Miao, Chu Ye, Weiqiang Yang, Wen Zhong, Jing Chen. Identification of QTLs for plant height and branching-related traits in cultivated peanut[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2511-2524.
[7] Chunxiang Li, Yongfeng Song, Yong Zhu, Mengna Cao, Xiao Han, Jinsheng Fan, Zhichao Lü, Yan Xu, Yu Zhou, Xing Zeng, Lin Zhang, Ling Dong, Dequan Sun, Zhenhua Wang, Hong Di. GWAS analysis reveals candidate genes associated with density tolerance (ear leaf structure) in maize (Zea mays L.)[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2046-2062.
[8] Berhane S. Gebregziabher, Shengrui Zhang, Jing Li, Bin Li, Junming Sun. Identification of genomic regions and candidate genes underlying carotenoid accumulation in soybean using next-generation sequen-cing based bulk segregant analysis[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2063-2079.
[9] Jie Zhang, Qi Wang, Jinxi Yuan, Zhen Tian, Shanchun Yan, Wei Liu.
Development of a piggyBac transgenic system in Bactrocera dorsalis and its potential for research on olfactory molecular targets
[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2311-2326.
[10] Huairen Zhang, Tauseef Taj Kiani, Huabang Chen, Juan Liu, Xunji Chen. Genome wide association analysis reveals multiple QTLs controlling root development in maize [J]. >Journal of Integrative Agriculture, 2025, 24(5): 1656-1670.
[11] Zipeng Zhang, Siyuan Xing, Ao Qiu, Ning Zhang, Wenwen Wang, Changsong Qian, Jia’nan Zhang, Chuduan Wang, Qin Zhang, Xiangdong Ding. The development of a porcine 50K SNP panel using genotyping by target sequencing and its application[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1930-1943.
[12] Yang Wang, Chunhua Mu, Xiangdong Li, Canxing Duan, Jianjun Wang, Xin Lu, Wangshu Li, Zhennan Xu, Shufeng Sun, Ao Zhang, Zhiqiang Zhou, Shenghui Wen, Zhuanfang Hao, Jienan Han, Jianzhou Qu, Wanli Du, Fenghai Li, Jianfeng Weng. A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize[J]. >Journal of Integrative Agriculture, 2025, 24(2): 453-466.
[13] Rui Liu, Hongna Cheng, Dandan Qin, Le Xu, Fuchao Xu, Qing Xu, Yanchun Peng, Shuangtao Ge, Longqing Sun, Guoqing Dong, Jing Dong. Functional characterization and identification of superior haplotypes of barley HvGL7-2H (Hordeum vulgare L.) in grain features[J]. >Journal of Integrative Agriculture, 2025, 24(11): 4153-4167.
[14] Mianyan Li, Lei Pu, David E. MacHugh, Jingjing Tian, Xiaoqing Wang, Qingyao Zhao, Lijun Shi, Hongmei Gao, Ying Yu, Lixian Wang, Fuping Zhao. Genome-wide association studies of novel resilience traits identify important immune QTL regions and candidate genes in Duroc pigs[J]. >Journal of Integrative Agriculture, 2025, 24(11): 4355-4369.
[15] Kaiyuan Ji, Yiwei Zhao, Xin Yuan, Chun’e Liang, Xueqing Zhang, Wenli Tian, Tong Yu, Yangyang Ma, Yinghui Ling, Yunhai Zhang. circKIF27 inhibits melanogenesis and proliferation by targeting miR-129-5p/TGIF2 pathway in goat melanocytes[J]. >Journal of Integrative Agriculture, 2025, 24(10): 3997-4011.
No Suggested Reading articles found!