Mitochondrial DNA The Journal of DNA Mapping, Sequencing, and Analysis
ISSN: 1940-1736 (Print) 1940-1744 (Online) Journal homepage: http://www.tandfonline.com/loi/imdn20
High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep Neena Amatya Gorkhali, Lin Jiang, Bhola Shankar Shrestha, Xiao-Hong He, Qian Junzhao, Jian-Lin Han & Yue-Hui Ma To cite this article: Neena Amatya Gorkhali, Lin Jiang, Bhola Shankar Shrestha, Xiao-Hong He, Qian Junzhao, Jian-Lin Han & Yue-Hui Ma (2015): High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep, Mitochondrial DNA To link to this article: http://dx.doi.org/10.3109/19401736.2015.1041134
Published online: 18 Jun 2015.
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Date: 26 September 2015, At: 20:57
http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–3 ! 2015 Informa UK Ltd. DOI: 10.3109/19401736.2015.1041134
SHORT COMMUNICATION
High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep Neena Amatya Gorkhali1,2, Lin Jiang1, Bhola Shankar Shrestha2, Xiao-Hong He1, Qian Junzhao1, Jian-Lin Han1,3, and Yue-Hui Ma1 1
Downloaded by [University of Otago] at 20:57 26 September 2015
CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China, 2Animal Breeding Division, National Animal Science Institute, Nepal Agriculture Research Council (NARC), Kathmandu, Nepal, and 3International Livestock Research Institute (ILRI), Nairobi, Kenya Abstract
Keywords
Heteroplasmy due to length polymorphism with tandem repeats in mtDNAs within individual was hardly studied in domestic animals. In the present study, we identified intra-individual length variation in the control region of mtDNAs in Nepalese sheep by molecular cloning and sequencing techniques. We observed one to four tandem repeats of a 75-bp nucleotide sequences in the mtDNA control region in 45% of the total Nepalese sheep sampled in contrast to the Chinese sheep, indicating that the heteroplasmy is specific to Nepalese sheep. The high rate of heteroplasmy in Nepalese sheep could be a resultant of the mtDNA mutation and independent segregation at intra-individual level or a strand slippage and mispairing during the replication.
Heteroplasmy, mtDNA control region, Nepalese sheep, tandem repeats
Introduction Heteroplasmy corresponding with tandemly repeated sequences within the control region of mitochondrial genome is universally accepted in mammals (Hayasaka et al., 1991) and birds (He et al., 2013). Tandem motifs of 75/76-bp were also found to exhibit a variable number of repeats among different mtDNAs, and thus heteroplasmy with respect to repeat number within a population of European sheep (Hiendleder et al., 1998). Similar intrapopulation length heteroplasmy has been reported in sheep from Asia including China (Li et al., 2006) and India (Singh et al., 2013). Tendency of having intra-individual heteroplasmy was indicated when deliberately more PCR products were loaded in agarose gel run under electrophoresis unit (Hiendleder et al., 2002). However, heteroplasmy within an individual has not been not fully investigated in domestic sheep. In this study, we report the first direct evidence of tandem repeats associated with hete roplasmy within an individual in Nepalese indigenous domestic sheep using cloning and sequencing techniques.
Material and methods Six samples of Nepalese Kage sheep (four females and two males) and 10 of Chinese sheep as control were taken for DNA extraction using the phenol/chloroform protocol (Sambrook et al., 2001). The 780 bp from the long mtDNA control region (from position 15,410 to 16,186 ± 4Ts) were amplified using primers: 15388F
Correspondence: Yue-Hui Ma and Jian-Lin Han, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China. Tel: 86-136-0117-5992 (Y-H Ma); 86-136-9920-4782 (J-L Han). E-mail: [email protected] (Y-H Ma); [email protected] (J-L Han)
History Received 5 March 2015 Revised 7 April 2015 Accepted 12 April 2015 Published online 18 June 2015
(50 -GCC CCA CTA TCA ACA CCC AAA G-30 ) and CD-774R (50 -AAT GGG CGA TTT TAG ATG AGA TGG C-30 ) and PCR amplicons were directly sequenced using primers: CR018-for (50 -ATC ATT ATC AAC GAT AC-30 ) and CR653-rev (50 -GAA GAA AGA ACC AGA TGC CT-30 ) following the procedure of Luo et al. (2005). To validate the occurrence of multiple bands observed in electrophoresis of the PCR products, amplified mtDNA control region fragments were directly sequenced. To avoid the most frequent amplicon from being sequenced, the PCR products (three Nepalese and one Chinese sheep samples) were further cloned according to the manufacturer’s protocol of pGM-T cloning kit (Tiangen Biotech C. Ltd, Beijing, China) and then sequenced by Sanger sequencing (Table 1). The raw sequencing profiles of mtDNA control region from each of the sequences were manually edited using program Chromas version 2.23 (http://www.technelysium.com.au/chromas2.html) and aligned using the Cluster W algorithm included in program MEGA version 5.0 (Tamura et al., 2011) to compare with the reference sequence [accession # AF010406 (Hiendleder et al., 1998)].
Results and discussion mtDNA sequence variation Direct sequencing showed all the mtDNA control region sequences from Nepalese sheep and Chinese sheep samples carried four tandem repeats of 75/76 bp nucleotides (50 -CGT ACA T(T/–)A GTA TTA ATG TAA TAT AGA CAT TAT ATG TAT AAA GTA CAT TAA ATG ATT TAC CCC ATG CAT ATA AGC A-30 ) with or without Thymine (T) insertion whereas our previous studies showed intra-population length polymorphism in Nepalese sheep (Gorkhali et al., 2014).
2
N. A. Gorkhali et al.
Mitochondrial DNA, Early Online: 1–3
Table 1. Number of tandem repeats within an individual. Tandem repeats Type Nepalese sheep Nepalese sheep Chinese sheep
Sample code KF2-2 KF3-2 KM2-2 Total
No. of sequences
4
3
2
1
Others
18 24 11 53 20
14 9 5 28 (66.7) 6 (100)
2 3 – 5 (11.9) –
1 3 4 8 (19.1) –
– 1 – 1 (2.3) –
1 8 2 11 14
Downloaded by [University of Otago] at 20:57 26 September 2015
Values in parenthesis are %.
Figure 1. Heteroplasmic individuals of the Nepalese sheep breed, Kage, shown in a 2.5% agarose gel with PCR amplified mtDNA control region. Marker 1 kb is in the either side of the gel and the Nepalese Kage breed sheep samples are KF2-2, KF4-2, KF5-2, KF6-2, KM1-2, and KM2-2 from left to right. The bands of around 800 bp are showing four tandem repeats.
Length polymorphism and heteroplasmy The cloning analysis revealed that all three Nepalese sheep samples chosen showed heteroplasmy with 2–4 different sequences with variations in tandem repeats within an individual (Table 1). Examination of the mtDNAs containing less than four tandem repeats revealed that in most cases the last tandem motif were missing whereas in one sequence of KF2-2, the second and third tandem motifs were missing, and in two sequences of KF2-2, the third tandem repeat was missing. Similar random deletion was also reported in Chinese sheep mtDNA D-loop region (Li et al., 2006). In the Chinese samples, all six cloned sequences exhibited four tandem repeats with no variation in tandem repeats. Surprisingly, about 70% of the total clones were unspecific amplifications (Table 1), probably because of the deterioration of the DNA material. Discarding unspecific PCR amplifications, both the Nepalese and the Chinese sheep populations showed high occurrence of four tandem repeats (Table 1), which is consistent to the earlier result on the general sheep mtDNA (Hiendleder et al., 1998). However, in Nepalese sheep exclusively, two tandem repeats (19.1%) are next to the highest, followed by three repeats (11.9%) and with one tandem motif (2.3%) (Table 1). These findings revealed that Nepalese sheep have more tendency of occurrence of heteroplasmy, compared with Chinese sheep. Furthermore, by examining the chromatograms of all sequences generated from the primers amplifying the control region escaping the tandem repeats (15,984–16,537 bp of the reference sequence, unpublished data), in 45% of all Nepalese sheep, we found high occurrence of base overlaps which probably corresponded with heteroplasmy (He et al., 2013), in contrast to clean ones obtained in Chinese sheep. This is consistent with the cloning results (Table 1) as both suggested that length heteroplasmy is specific to Nepalese sheep. Furthermore, this finding is reinforced by multiple bands observed in the agarose gel
(Figure 1) in all the Nepalese representative samples which clearly shows the high occurrence of intra-individual heteroplasmy in Nepalese sheep. Length polymorphism within population is not unusual in the animal mtDNA. However, heteroplasmy in sheep at such high frequency was not reported earlier (Hiendleder et al., 1998; Wood & Phua, 1996). Surprisingly, Luo et al. (2005) have not reported any heteroplasmy despite the same set of primers and PCR conditions. This also indicated less prevalence of the heteroplasmy in Chinese breeds. The higher occurrence of heteroplasmy in Nepalese sheep could be due to the mtDNA mutation and independent segregation at intra-individual level (Wallace & Chalkia, 2013) and/or can have a strand slippage and mispairing during replication; this mechanism for heteroplasmy was well described in heteroplasmy in other mammals (Wilkinson & Chapman, 1991) with similar length size of tandem repeats that are close to the promoter region and the origin of the replication of mtDNA (Clayton, 2000; Falkenberg, 2007).
Conclusion From the present study, we can conclude that the Nepalese sheep population is highly heteroplasmic with up to four different variations in one individual. The heteroplasmy might be due to the mtDNA mutation at intra-individual level and/or the replication slippage. However, the complete mechanism for the high rate of heteroplasmy in the Nepalese sheep is still not clear. A comprehensive investigation with larger population size is warranted.
Acknowledgements The authors wish to thank the staff of Animal Breeding Division for their assistance in collecting samples.
DOI: 10.3109/19401736.2015.1041134
Declaration of interest The authors report no conflicts of interests. The authors alone are responsible for the content and writing of this article. This work was supported by the National Natural Science Foundation of China (31272403) and the Agricultural Science and Technology Innovation Program of China (ASTIP-IAS01).
Downloaded by [University of Otago] at 20:57 26 September 2015
References Clayton D. (2000). Transcription and replication of mitochondrial DNA. Hum Reprod 15:11–17. Falkenberg M, Larsson NG, Gustafsson CM. (2007). DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679–99. Gorkhali NA, Han J-L, Ma Y-H. (2014). Mitochondrial DNA variation in indigenous sheep (Ovis aries) breeds of Nepal. Proceeding of the twenty sixth annual congress of the Post Graduate Institute of Agriculture (PGIA) 26:3 (Abstract). Hayasaka K, Ishida T, Horai S. (1991). Heteroplasmy and polymorphism in the major non-coding region of mitochondrial DNA in Japanese monkeys: Association with tandemly repeated sequences. Mol Biol Evol 8:399–415. He X-L, Ding C-Q, Han J-L. (2013). Lack of structural variation but extensive length polymorphisms and heteroplasmic length variations in the mitochondrial DNA control region of highly inbred Crested Ibis, Nipponia nippon. PLoS One 8:e66324. Hiendleder S, Kaupe B, Wassmuth R, Janke A. (2002). Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proc R Soc Lond 269:893–904.
Heteroplasmy in mitochondrial DNA
3
Hiendleder S, Lewalski H, Wassmuth R, Janke A. (1998). The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major ovine haplotype. J Mol Evol 47: 441–8. Li X-L, Gong Y-F, Liu Z-Z, Zheng G-R, Zhou R-Y, Jin X-M, Li L-H, Wang H-L. (2006). Study on tandem repeat sequence variation in sheep mtDNA D-loop region. Acta Genetica Sinica 33:1087–95. Luo Y-Z, Cheng S-R, Lkhagva B, Badamdorji D, Hanotte O, Han J-L. (2005). Origin and genetic diversity of Mongolian and Chinese sheep using mitochondrial DNA D-loop sequences. Acta Genetica Sinica 32: 1256–65. Sambrook J, Fritsch EF, Maniatis T. (2001). Molecular cloning: A laboratory manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Singh S, Kumar Jr S, Kolte AP, Kumar S. (2013). Extensive variation and sub-structuring in lineage A mtDNA in Indian sheep: Genetic evidence for domestication of sheep in India. PLoS One 8: e77858. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol l28:2731–9. Wallace DC, Chalkia D. (2013). Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol 5:a021220. Wilkinson GS, Chapman AM. (1991). Length and sequence variation in evening bat D-loop mtDNA. Genetics 128:607–17. Wood NJ, Phua SH. (1996). Variation in the control region sequence of the sheep mitochondrial genome. Anim Genet 27: 25–33.
ISSN: 1940-1736 (Print) 1940-1744 (Online) Journal homepage: http://www.tandfonline.com/loi/imdn20
High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep Neena Amatya Gorkhali, Lin Jiang, Bhola Shankar Shrestha, Xiao-Hong He, Qian Junzhao, Jian-Lin Han & Yue-Hui Ma To cite this article: Neena Amatya Gorkhali, Lin Jiang, Bhola Shankar Shrestha, Xiao-Hong He, Qian Junzhao, Jian-Lin Han & Yue-Hui Ma (2015): High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep, Mitochondrial DNA To link to this article: http://dx.doi.org/10.3109/19401736.2015.1041134
Published online: 18 Jun 2015.
Submit your article to this journal
Article views: 15
View related articles
View Crossmark data
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=imdn20 Download by: [University of Otago]
Date: 26 September 2015, At: 20:57
http://informahealthcare.com/mdn ISSN: 1940-1736 (print), 1940-1744 (electronic) Mitochondrial DNA, Early Online: 1–3 ! 2015 Informa UK Ltd. DOI: 10.3109/19401736.2015.1041134
SHORT COMMUNICATION
High occurrence of mitochondrial heteroplasmy in nepalese indigenous sheep (Ovis aries) compared to chinese sheep Neena Amatya Gorkhali1,2, Lin Jiang1, Bhola Shankar Shrestha2, Xiao-Hong He1, Qian Junzhao1, Jian-Lin Han1,3, and Yue-Hui Ma1 1
Downloaded by [University of Otago] at 20:57 26 September 2015
CAAS-ILRI Joint Laboratory on Livestock and Forage Genetic Resources, Institute of Animal Science, Chinese Academy of Agricultural Sciences (CAAS), Beijing, China, 2Animal Breeding Division, National Animal Science Institute, Nepal Agriculture Research Council (NARC), Kathmandu, Nepal, and 3International Livestock Research Institute (ILRI), Nairobi, Kenya Abstract
Keywords
Heteroplasmy due to length polymorphism with tandem repeats in mtDNAs within individual was hardly studied in domestic animals. In the present study, we identified intra-individual length variation in the control region of mtDNAs in Nepalese sheep by molecular cloning and sequencing techniques. We observed one to four tandem repeats of a 75-bp nucleotide sequences in the mtDNA control region in 45% of the total Nepalese sheep sampled in contrast to the Chinese sheep, indicating that the heteroplasmy is specific to Nepalese sheep. The high rate of heteroplasmy in Nepalese sheep could be a resultant of the mtDNA mutation and independent segregation at intra-individual level or a strand slippage and mispairing during the replication.
Heteroplasmy, mtDNA control region, Nepalese sheep, tandem repeats
Introduction Heteroplasmy corresponding with tandemly repeated sequences within the control region of mitochondrial genome is universally accepted in mammals (Hayasaka et al., 1991) and birds (He et al., 2013). Tandem motifs of 75/76-bp were also found to exhibit a variable number of repeats among different mtDNAs, and thus heteroplasmy with respect to repeat number within a population of European sheep (Hiendleder et al., 1998). Similar intrapopulation length heteroplasmy has been reported in sheep from Asia including China (Li et al., 2006) and India (Singh et al., 2013). Tendency of having intra-individual heteroplasmy was indicated when deliberately more PCR products were loaded in agarose gel run under electrophoresis unit (Hiendleder et al., 2002). However, heteroplasmy within an individual has not been not fully investigated in domestic sheep. In this study, we report the first direct evidence of tandem repeats associated with hete roplasmy within an individual in Nepalese indigenous domestic sheep using cloning and sequencing techniques.
Material and methods Six samples of Nepalese Kage sheep (four females and two males) and 10 of Chinese sheep as control were taken for DNA extraction using the phenol/chloroform protocol (Sambrook et al., 2001). The 780 bp from the long mtDNA control region (from position 15,410 to 16,186 ± 4Ts) were amplified using primers: 15388F
Correspondence: Yue-Hui Ma and Jian-Lin Han, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China. Tel: 86-136-0117-5992 (Y-H Ma); 86-136-9920-4782 (J-L Han). E-mail: [email protected] (Y-H Ma); [email protected] (J-L Han)
History Received 5 March 2015 Revised 7 April 2015 Accepted 12 April 2015 Published online 18 June 2015
(50 -GCC CCA CTA TCA ACA CCC AAA G-30 ) and CD-774R (50 -AAT GGG CGA TTT TAG ATG AGA TGG C-30 ) and PCR amplicons were directly sequenced using primers: CR018-for (50 -ATC ATT ATC AAC GAT AC-30 ) and CR653-rev (50 -GAA GAA AGA ACC AGA TGC CT-30 ) following the procedure of Luo et al. (2005). To validate the occurrence of multiple bands observed in electrophoresis of the PCR products, amplified mtDNA control region fragments were directly sequenced. To avoid the most frequent amplicon from being sequenced, the PCR products (three Nepalese and one Chinese sheep samples) were further cloned according to the manufacturer’s protocol of pGM-T cloning kit (Tiangen Biotech C. Ltd, Beijing, China) and then sequenced by Sanger sequencing (Table 1). The raw sequencing profiles of mtDNA control region from each of the sequences were manually edited using program Chromas version 2.23 (http://www.technelysium.com.au/chromas2.html) and aligned using the Cluster W algorithm included in program MEGA version 5.0 (Tamura et al., 2011) to compare with the reference sequence [accession # AF010406 (Hiendleder et al., 1998)].
Results and discussion mtDNA sequence variation Direct sequencing showed all the mtDNA control region sequences from Nepalese sheep and Chinese sheep samples carried four tandem repeats of 75/76 bp nucleotides (50 -CGT ACA T(T/–)A GTA TTA ATG TAA TAT AGA CAT TAT ATG TAT AAA GTA CAT TAA ATG ATT TAC CCC ATG CAT ATA AGC A-30 ) with or without Thymine (T) insertion whereas our previous studies showed intra-population length polymorphism in Nepalese sheep (Gorkhali et al., 2014).
2
N. A. Gorkhali et al.
Mitochondrial DNA, Early Online: 1–3
Table 1. Number of tandem repeats within an individual. Tandem repeats Type Nepalese sheep Nepalese sheep Chinese sheep
Sample code KF2-2 KF3-2 KM2-2 Total
No. of sequences
4
3
2
1
Others
18 24 11 53 20
14 9 5 28 (66.7) 6 (100)
2 3 – 5 (11.9) –
1 3 4 8 (19.1) –
– 1 – 1 (2.3) –
1 8 2 11 14
Downloaded by [University of Otago] at 20:57 26 September 2015
Values in parenthesis are %.
Figure 1. Heteroplasmic individuals of the Nepalese sheep breed, Kage, shown in a 2.5% agarose gel with PCR amplified mtDNA control region. Marker 1 kb is in the either side of the gel and the Nepalese Kage breed sheep samples are KF2-2, KF4-2, KF5-2, KF6-2, KM1-2, and KM2-2 from left to right. The bands of around 800 bp are showing four tandem repeats.
Length polymorphism and heteroplasmy The cloning analysis revealed that all three Nepalese sheep samples chosen showed heteroplasmy with 2–4 different sequences with variations in tandem repeats within an individual (Table 1). Examination of the mtDNAs containing less than four tandem repeats revealed that in most cases the last tandem motif were missing whereas in one sequence of KF2-2, the second and third tandem motifs were missing, and in two sequences of KF2-2, the third tandem repeat was missing. Similar random deletion was also reported in Chinese sheep mtDNA D-loop region (Li et al., 2006). In the Chinese samples, all six cloned sequences exhibited four tandem repeats with no variation in tandem repeats. Surprisingly, about 70% of the total clones were unspecific amplifications (Table 1), probably because of the deterioration of the DNA material. Discarding unspecific PCR amplifications, both the Nepalese and the Chinese sheep populations showed high occurrence of four tandem repeats (Table 1), which is consistent to the earlier result on the general sheep mtDNA (Hiendleder et al., 1998). However, in Nepalese sheep exclusively, two tandem repeats (19.1%) are next to the highest, followed by three repeats (11.9%) and with one tandem motif (2.3%) (Table 1). These findings revealed that Nepalese sheep have more tendency of occurrence of heteroplasmy, compared with Chinese sheep. Furthermore, by examining the chromatograms of all sequences generated from the primers amplifying the control region escaping the tandem repeats (15,984–16,537 bp of the reference sequence, unpublished data), in 45% of all Nepalese sheep, we found high occurrence of base overlaps which probably corresponded with heteroplasmy (He et al., 2013), in contrast to clean ones obtained in Chinese sheep. This is consistent with the cloning results (Table 1) as both suggested that length heteroplasmy is specific to Nepalese sheep. Furthermore, this finding is reinforced by multiple bands observed in the agarose gel
(Figure 1) in all the Nepalese representative samples which clearly shows the high occurrence of intra-individual heteroplasmy in Nepalese sheep. Length polymorphism within population is not unusual in the animal mtDNA. However, heteroplasmy in sheep at such high frequency was not reported earlier (Hiendleder et al., 1998; Wood & Phua, 1996). Surprisingly, Luo et al. (2005) have not reported any heteroplasmy despite the same set of primers and PCR conditions. This also indicated less prevalence of the heteroplasmy in Chinese breeds. The higher occurrence of heteroplasmy in Nepalese sheep could be due to the mtDNA mutation and independent segregation at intra-individual level (Wallace & Chalkia, 2013) and/or can have a strand slippage and mispairing during replication; this mechanism for heteroplasmy was well described in heteroplasmy in other mammals (Wilkinson & Chapman, 1991) with similar length size of tandem repeats that are close to the promoter region and the origin of the replication of mtDNA (Clayton, 2000; Falkenberg, 2007).
Conclusion From the present study, we can conclude that the Nepalese sheep population is highly heteroplasmic with up to four different variations in one individual. The heteroplasmy might be due to the mtDNA mutation at intra-individual level and/or the replication slippage. However, the complete mechanism for the high rate of heteroplasmy in the Nepalese sheep is still not clear. A comprehensive investigation with larger population size is warranted.
Acknowledgements The authors wish to thank the staff of Animal Breeding Division for their assistance in collecting samples.
DOI: 10.3109/19401736.2015.1041134
Declaration of interest The authors report no conflicts of interests. The authors alone are responsible for the content and writing of this article. This work was supported by the National Natural Science Foundation of China (31272403) and the Agricultural Science and Technology Innovation Program of China (ASTIP-IAS01).
Downloaded by [University of Otago] at 20:57 26 September 2015
References Clayton D. (2000). Transcription and replication of mitochondrial DNA. Hum Reprod 15:11–17. Falkenberg M, Larsson NG, Gustafsson CM. (2007). DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679–99. Gorkhali NA, Han J-L, Ma Y-H. (2014). Mitochondrial DNA variation in indigenous sheep (Ovis aries) breeds of Nepal. Proceeding of the twenty sixth annual congress of the Post Graduate Institute of Agriculture (PGIA) 26:3 (Abstract). Hayasaka K, Ishida T, Horai S. (1991). Heteroplasmy and polymorphism in the major non-coding region of mitochondrial DNA in Japanese monkeys: Association with tandemly repeated sequences. Mol Biol Evol 8:399–415. He X-L, Ding C-Q, Han J-L. (2013). Lack of structural variation but extensive length polymorphisms and heteroplasmic length variations in the mitochondrial DNA control region of highly inbred Crested Ibis, Nipponia nippon. PLoS One 8:e66324. Hiendleder S, Kaupe B, Wassmuth R, Janke A. (2002). Molecular analysis of wild and domestic sheep questions current nomenclature and provides evidence for domestication from two different subspecies. Proc R Soc Lond 269:893–904.
Heteroplasmy in mitochondrial DNA
3
Hiendleder S, Lewalski H, Wassmuth R, Janke A. (1998). The complete mitochondrial DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major ovine haplotype. J Mol Evol 47: 441–8. Li X-L, Gong Y-F, Liu Z-Z, Zheng G-R, Zhou R-Y, Jin X-M, Li L-H, Wang H-L. (2006). Study on tandem repeat sequence variation in sheep mtDNA D-loop region. Acta Genetica Sinica 33:1087–95. Luo Y-Z, Cheng S-R, Lkhagva B, Badamdorji D, Hanotte O, Han J-L. (2005). Origin and genetic diversity of Mongolian and Chinese sheep using mitochondrial DNA D-loop sequences. Acta Genetica Sinica 32: 1256–65. Sambrook J, Fritsch EF, Maniatis T. (2001). Molecular cloning: A laboratory manual. 3rd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. Singh S, Kumar Jr S, Kolte AP, Kumar S. (2013). Extensive variation and sub-structuring in lineage A mtDNA in Indian sheep: Genetic evidence for domestication of sheep in India. PLoS One 8: e77858. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol l28:2731–9. Wallace DC, Chalkia D. (2013). Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol 5:a021220. Wilkinson GS, Chapman AM. (1991). Length and sequence variation in evening bat D-loop mtDNA. Genetics 128:607–17. Wood NJ, Phua SH. (1996). Variation in the control region sequence of the sheep mitochondrial genome. Anim Genet 27: 25–33.
