Skip to main content Accessibility help

New insights into mitogenomic phylogeny and copy number in eight indigenous sheep populations based on the ATP synthase and cytochrome c oxidase genes

  • P. Xiao (a1), L. L. Niu (a1), Q. J. Zhao (a2), X. Y. Chen (a3), L. J. Wang (a1), L. Li (a1), H. P. Zhang (a1), J. Z. Guo (a1), H. Y. Xu (a1) and T. Zhong (a1)...


The origins and phylogeny of different sheep breeds has been widely studied using polymorphisms within the mitochondrial hypervariable region. However, little is known about the mitochondrial DNA (mtDNA) content and phylogeny based on mtDNA protein-coding genes. In this study, we assessed the phylogeny and copy number of the mtDNA in eight indigenous (population size, n=184) and three introduced (n=66) sheep breeds in China based on five mitochondrial coding genes (COX1, COX2, ATP8, ATP6 and COX3). The mean haplotype and nucleotide diversities were 0.944 and 0.00322, respectively. We identified a correlation between the lineages distribution and the genetic distance, whereby Valley-type Tibetan sheep had a closer genetic relationship with introduced breeds (Dorper, Poll Dorset and Suffolk) than with other indigenous breeds. Similarly, the Median-joining profile of haplotypes revealed the distribution of clusters according to genetic differences. Moreover, copy number analysis based on the five mitochondrial coding genes was affected by the genetic distance combining with genetic phylogeny; we also identified obvious non-synonymous mutations in ATP6 between the different levels of copy number expressions. These results imply that differences in mitogenomic compositions resulting from geographical separation lead to differences in mitochondrial function.


Corresponding author



Hide All
Anderson, S, Bankier, AT, Barrell, BG, de Bruijn, MH, Coulson, AR, Drouin, J, Eperon, IC, Nierlich, DP, Roe, BA, Sanger, F, Schreier, PH, Smith, AJ, Staden, R and Young, IG 1981. Sequence and organization of the human mitochondrial genome. Nature 290, 457465.
Ballester, M, Castello, A, Ibanez, E, Sanchez, A and Folch, JM 2004. Real-time quantitative PCR-based system for determining transgene copy number in transgenic animals. Biotechniques 37, 610613.
Bandelt, HJ, Forster, P and Rohl, A 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.
Behera, BK, Kunal, SP, Paria, P, Das, P, Meena, DK, Pakrashi, S, Sahoo, AK, Panda, D, Jena, J and Sharma, AP 2015. Genetic differentiation in Indian Major Carp, Cirrhinus mrigala (Hamilton, 1822) from Indian Rivers, as revealed by direct sequencing analysis of mitochondrial Cytochrome b region. Mitochondrial DNA 26, 334336.
Camus, MF, Wolf, JB, Morrow, EH and Dowling, DK 2015. Single nucleotides in the mtDNA sequence modify mitochondrial molecular function and are associated with sex-specific effects on fertility and aging. Current Biology 25, 27172722.
Carneiro, M, Afonso, S, Geraldes, A, Garreau, H, Bolet, G, Boucher, S, Tircazes, A, Queney, G, Nachman, MW and Ferrand, N 2011. The genetic structure of domestic rabbits. Molecular Biology and Evolution 28, 18011816.
Chen, SY, Duan, ZY, Sha, T, Xiangyu, J, Wu, SF and Zhang, YP 2006. Origin, genetic diversity, and population structure of Chinese domestic sheep. Gene 376, 216223.
Delrieu-Trottin, E, Mona, S, Maynard, J, Neglia, V, Veuille, M and Planes, S 2017. Population expansions dominate demographic histories of endemic and widespread Pacific reef fishes. Scientific Reports 7, 40519.
Excoffier, L and Lischer, HE 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.
Ferguson-Miller, S and Babcock, GT 1996. Heme/copper terminal oxidases. Chemical Reviews 96, 28892908.
Hartmann, N, Reichwald, K, Wittig, I, Drose, S, Schmeisser, S, Luck, C, Hahn, C, Graf, M, Gausmann, U, Terzibasi, E, Cellerino, A, Ristow, M, Brandt, U, Platzer, M and Englert, C 2011. Mitochondrial DNA copy number and function decrease with age in the short-lived fish Nothobranchius furzeri . Aging Cell 10, 824831.
Jiang, L, Zhang, S, Dong, C, Chen, B, Feng, J, Peng, W, Mahboob, S, Al-Ghanim, KA and Xu, P 2016. Genome-wide identification, phylogeny, and expression of fibroblast growth genes in common carp. Gene 578, 225231.
Joy, L, Mohitha, C, Divya, PR, Gopalakrishnan, A, Basheer, VS and Jena, JK 2016. Weak genetic differentiation in cobia, Rachycentron canadum from Indian waters as inferred from mitochondrial DNA ATPase 6 and 8 genes. Mitochondrial DNA. Part A, DNA Mapping, Sequencing and Analysis 27, 28192821.
Kersten, B, Faivre Rampant, P, Mader, M, Le Paslier, MC, Bounon, R, Berard, A, Vettori, C, Schroeder, H, Leple, JC and Fladung, M 2016. Genome sequences of Populus tremula chloroplast and mitochondrion: implications for holistic poplar breeding. PLoS One 11, e0147209.
Kibegwa, FM, Githui, KE, Jung’a, JO, Badamana, MS and Nyamu, MN 2016. Mitochondrial DNA variation of indigenous goats in Narok and Isiolo counties of Kenya. Journal of Animal Breeding and Genetics 133, 238247.
Liao, K, Yan, J, Mai, K and Ai, Q 2016. Dietary lipid concentration affects liver mitochondrial DNA copy number, gene expression and DNA methylation in large yellow croaker (Larimichthys crocea). Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 193, 2532.
Lv, FH, Peng, WF, Yang, J, Zhao, YX, Li, WR, Liu, MJ, Ma, YH, Zhao, QJ, Yang, GL, Wang, F, Li, JQ, Liu, YG, Shen, ZQ, Zhao, SG, Hehua, E, Gorkhali, NA, Farhad Vahidi, SM, Muladno, M, Naqvi, AN, Tabell, J, Iso-Touru, T, Bruford, MW, Kantanen, J, Han, JL and Li, MH 2015. Mitogenomic meta-analysis identifies two phases of migration in the history of Eastern Eurasian sheep. Molecular Biology and Evolution 32, 25152533.
Mahami-Oskouei, M, Kaseb-Yazdanparast, A, Spotin, A, Shahbazi, A, Adibpour, M, Ahmadpour, E and Ghabouli-Mehrabani, N 2016. Gene flow for Echinococcus granulosus metapopulations determined by mitochondrial sequences: a reliable approach for reflecting epidemiological drift of parasite among neighboring countries. Experimental Parasitology 171, 7783.
Mason, IL 1984. Evolution of domesticated animals. Longman, London, New York.
Meadows, JR, Cemal, I, Karaca, O, Gootwine, E and Kijas, JW 2007. Five ovine mitochondrial lineages identified from sheep breeds of the near East. Genetics 175, 13711379.
Meadows, JR, Hiendleder, S and Kijas, JW 2011. Haplogroup relationships between domestic and wild sheep resolved using a mitogenome panel. Heredity (Edinb) 106, 700706.
Niemi, M, Blauer, A, Iso-Touru, T, Harjula, J, Nystrom Edmark, V, Rannamae, E, Lougas, L, Sajantila, A, Liden, K and Taavitsainen, JP 2015. Temporal fluctuation in North East Baltic Sea region cattle population revealed by mitochondrial and Y-chromosomal DNA analyses. PLoS One 10, e0123821.
Nijtmans, LG, Klement, P, Houstek, J and van den Bogert, C 1995. Assembly of mitochondrial ATP synthase in cultured human cells: implications for mitochondrial diseases. Biochimica et Biophysica Acta 1272, 190198.
Niu, L, Chen, X, Xiao, P, Zhao, Q, Zhou, J, Hu, J, Sun, H, Guo, J, Li, L, Wang, L, Zhang, H and Zhong, T 2016. Detecting signatures of selection within the Tibetan sheep mitochondrial genome. Mitochondrial DNA. Part A, DNA Mapping, Sequencing, and Analysis 28, 19.
Pedrosa, S, Uzun, M, Arranz, JJ, Gutierrez-Gil, B, San Primitivo, F and Bayon, Y 2005. Evidence of three maternal lineages in near Eastern sheep supporting multiple domestication events. Proceedings. Biological Sciences 272, 22112217.
Rak, M, Benit, P, Chretien, D, Bouchereau, J, Schiff, M, El-Khoury, R, Tzagoloff, A and Rustin, P 2016. Mitochondrial cytochrome c oxidase deficiency. Clinical Science 130, 393407.
Ramadan, HA and El-Hefnawi, MM 2008. Phylogenetic analysis and comparison between cow and buffalo (including Egyptian buffaloes) mitochondrial displacement-loop regions. Mitochondrial DNA 19, 401410.
Resende, A, Goncalves, J, Muigai, AW and Pereira, F 2016. Mitochondrial DNA variation of domestic sheep (Ovis aries) in Kenya. Animal Genetics 47, 377381.
Rozas, J 2009. DNA sequence polymorphism analysis using DnaSP. Methods in Molecular Biology 537, 337350.
Sperl, W, Jesina, P, Zeman, J, Mayr, JA, Demeirleir, L, VanCoster, R, Pickova, A, Hansikova, H, Houst’kova, H, Krejcik, Z, Koch, J, Smet, J, Muss, W, Holme, E and Houstek, J 2006. Deficiency of mitochondrial ATP synthase of nuclear genetic origin. Neuromuscular Disorders 16, 821829.
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M and Kumar, S 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.
Wang, Y, Shen, Y, Feng, C, Zhao, K, Song, Z, Zhang, Y, Yang, L and He, S 2016. Mitogenomic perspectives on the origin of Tibetan loaches and their adaptation to high altitude. Scientific Reports 6, 29690.
Workalemahu, T, Enquobahrie, DA, Tadesse, MG, Hevner, K, Gelaye, B, Sanchez, SE and Williams, MA 2017. Genetic variations related to maternal whole blood mitochondrial DNA copy number: a genome-wide and candidate gene study. Journal of Maternal–Fetal & Neonatal Medicine 30, 17.
Yuan, Y, Wang, W, Li, H, Yu, Y, Tao, J, Huang, S and Zeng, Z 2015. Nonsense and missense mutation of mitochondrial ND6 gene promotes cell migration and invasion in human lung adenocarcinoma. BMC Cancer 15, 346.
Zeder, MA 2008. Domestication and early agriculture in the Mediterranean Basin: origins, diffusion, and impact. Proceedings of National Academy of Sciences USA 105, 1159711604.


Related content

Powered by UNSILO
Type Description Title
Supplementary materials

Xiao et al supplementary material
Figure S1

 Unknown (31 KB)
31 KB
Supplementary materials

Xiao et al supplementary material
Figure S2

 Unknown (145 KB)
145 KB
Supplementary materials

Xiao et al supplementary material
Figure S3

 Unknown (132 KB)
132 KB
Supplementary materials

Xiao et al supplementary material
Table S1

 Word (56 KB)
56 KB
Supplementary materials

Xiao et al supplementary material
Table S2

 Excel (164 KB)
164 KB
Supplementary materials

Xiao et al supplementary material
Table S3

 Word (51 KB)
51 KB
Supplementary materials

Xiao et al supplementary material
Table S4

 Excel (28 KB)
28 KB
Supplementary materials

Xiao et al supplementary material
Table S5

 Word (73 KB)
73 KB
Supplementary materials

Xiao et al supplementary material
Table S6

 Word (39 KB)
39 KB

New insights into mitogenomic phylogeny and copy number in eight indigenous sheep populations based on the ATP synthase and cytochrome c oxidase genes

  • P. Xiao (a1), L. L. Niu (a1), Q. J. Zhao (a2), X. Y. Chen (a3), L. J. Wang (a1), L. Li (a1), H. P. Zhang (a1), J. Z. Guo (a1), H. Y. Xu (a1) and T. Zhong (a1)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.