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The primary structure of COMT gene is not involved in the diet shift of the giant or the red pandas
Gene 562 (2015) 244–246
Contents lists available at ScienceDirect
Gene journal homepage: www.elsevier.com/locate/gene
Letter to the Editor The primary structure of COMT gene is not involved in the diet shift of the giant or the red pandas Keywords: COMT Diet shift Giant panda Red panda
Dear Editor, The giant panda (Ailuropoda melanoleuca) is an endangered species in China. As one species of family Ursidae order Carnivore, the giant panda has a very special bamboo diet, which is different from carnivores or omnivores of this order. That makes evolutionists so interested in the giant panda. Approximately 7 Ma ago, the ancient giant panda was still omnivorous (Jin et al., 2007). However, after 4.6 Ma to 5 Ma of evolution, the giant panda became herbivores and mainly feed on soft bamboo shoots, stems, and leaves (Jin et al., 2007). The modern giant panda consumes bamboos everyday, which account for 99% of its diet (Zhao et al., 2010). What's more, the giant panda also developed an enlarged radial sesamoid that functions as a thumb to grab bamboo (Jin et al., 2011). However, the giant panda possesses a more similar gastrointestinal tract type to those of carnivores than herbivores (Li et al., 2009). In other words, the digestive system of giant panda is more suitable for a meat diet than a bamboo diet. Worst of all, the giant panda lack the putative genes encoding for enzymes degrading lignocelluloses, which is the dominating component of bamboo (Li et al., 2009). Therefore, what is the real driving force that makes the giant panda diet switch is still an interesting question. Recently, several groups have attempted to characterize the cause of the giant panda diet switch. One of these groups reported that the T1R1 gene in the giant panda genome turned to be a pseudogene due to two frame-shifting mutations in exon 3 and exon 6, respectively (Li et al., 2009). T1R1 belongs to the vertebrate T1R family that comprises of three members in most species, and T1R1 and T1R3 form a heterodimer receptor that mediates the umami taste, which is the taste of glutamic acid and other amino acids (Nelson et al., 2002). But in bamboo amino acids level are less than in animal tissues (Kozukue et al., 1983). Thus another paper suggested that the lost function of T1R1 may result in the giant panda diet switch (Zhao et al., 2010). Furthermore, they found that T1R1 is intact in carnivores except giant panda. However, the T1R1 gene is also intact in some herbivorous such as cow and horse, which implies that the pseudogenization of T1R1 may not be the only reason for the giant panda eating bamboo.
Abbreviations: COMT, catechol-o-methyltransferase, T1R1, taste receptor type 1 member 1, T1R3, taste receptor type 1 member 3, SAM, S-adenosyl methionine.
http://dx.doi.org/10.1016/j.gene.2015.02.046 0378-1119/© 2015 Elsevier B.V. All rights reserved.
Another group proposed that the distinctive COMT is responsible for the giant panda's food choice by a comprehensive analysis (Jin et al., 2011). COMT is an enzyme that degrades catecholamines such as dopamine, epinephrine, and norepinephrine. The enzyme introduces a methyl group to the catecholamine, which is donated by the methionine portion of SAM. In human COMT, the methionine portion of SAM is fixed in the right place by hydrogen bonds with several vital residues in α3, α4, and β4 (Rutherford et al., 2008). Firstly, compared with other eight species, the predicted COMT protein appeared four amino acid deletions in giant panda, leading to an important change from the α4 helix to a more flexible loop in the panda's COMT structure (Jin et al., 2011). Such structural variation of the giant panda's COMT may have a relatively weak effect on inactivating catecholamines. Secondly, focusing on the Kozak consensus sequence, they observed that COMT in giant panda had a weaker Kozak motif (Jin et al., 2011). That may cause a lower expression of COMT, and probably can further enhance the effect of its coding region. Thirdly, in the post-transcription regulation level, the 3′UTR of COMT gene was predicted to be regulated by miR-199a-5p in giant panda but not in human (Jin et al., 2011). The predicted miRNA regulation may reduce the mRNA level of COMT. To some extent, it enhances the catecholamine level. Previous studies indicated that COMTdeficient male mice had promoted dopamine levels (Huotari et al., 2002), which could improve appetite in mice (Wise, 2004). And some papers found that several mutations of COMT were connected with eating disorders in human (Mikolajczyk et al., 2010; Yilmaz et al., 2011; Groleau et al., 2012; Favaro et al., 2013). Hence, it is very possible that the potential lower activity of COMT in giant panda is associated with its eating bamboo diet. Red panda (Ailurus fulgens) is the only living species of the genus Ailurus and the family Ailuridae. Like the giant panda, the red panda also regards the bamboo as its major food source, which occupies over 90% of its diet (Glatston, 2010). However, because its digestive system is relatively short and simple, the red panda also can't process bamboo well. Therefore, we hypothesized that the COMT may be related to the red panda diet switch, like giant panda. In this study, firstly, we collected one blood sample of giant panda (Giant panda 1) from the China Conservation and Research Center for the Giant Panda, Ya'an, Sichuan Province, China, and one muscle sample (Red panda 1) from a dead red panda found in the Fengtongzhai National Nature Reserve (Baoxing, Sichuan Province, China), both blood and tissue samples were stored at − 20 °C before use. DNA was extracted from these samples by using the TIANamp Genomic DNA Kit according to the manufacturer's protocol. Based on multiple sequence alignment of COMT coding region from nine mammals (Table S1), we designed one pair of specific primers (Table S2) for amplifying the interesting region of COMT gene. PCR products were then cloned into pEASY-T1 Simple Cloning vector. Two colonies for each sample were picked and their plasmids were sequenced by Invitrogen Company. Surprisingly, neither the giant panda nor the red panda showed a four amino acids' deletion in the COMT region (Fig. 1A), which was reported to have involved in the diet shift in giant panda (Jin et al., 2011). Based on our results, we supposed that the deletions may due to the polymorphism
Letter to the Editor
245
Giant panda
Fig. 1. COMT gene is intact both in giant panda and red panda. A: Alignment of the partial amino acids of COMT in nine species. Giant panda 1, Giant panda 2, Red panda 1, and Red panda 2 were sequenced by this study, all other sequences were downloaded from Ensemble. B: Comparison diagram of COMT gene in giant panda and dog. The red box refers to the coding exon and the white box stands for the intron. C: Alignment of the second coding exon in ten species. The sequence of giant panda (downloaded) was comprised of the second coding exon, the second intron, and the third coding exon.
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of the COMT among individuals of the giant and red pandas, or the genome sequencing error in the giant panda. To further determine if there are polymorphisms in COMT gene, we collected two fecal samples from giant panda (Giant panda 2) and red panda (Red panda 2), respectively. Another pair of specific primers (Table S2) was designed. DNA sequencing results showed that the COMT genes of giant panda and red panda both still possessed the four amino acids (Fig. 1A), which formed the important α4 helix. Therefore, the 4 amino acid deletion genotype of the COMT, if it exists, is not dominant, and thus can hardly explain the diet shift of the giant or red panda. While it's possible that the 12 nucleotides missing of the COMT in giant panda are artificial and caused by the genome sequencing mistake. The COMT gene in giant panda has five coding exons and four introns, but in dog' COMT there are only four coding exons and three introns (Fig. 1B). Moreover, the deletion happened between the second coding exon and the third coding exon in giant panda. And it was strange that the second intron of COMT gene only had a single A in giant panda genome. Thus we speculated that there was no intron between the second coding exon and the third coding exon. In other words, COMT has four coding exons in giant panda as well. To confirm this prediction, we compared the second coding exon of COMT gene of giant panda with that of other eight species. The result clearly showed that COMT gene indeed in giant panda had no difference with other species' COMT (Fig. 1C) in terms of the exon–intron structure. Hence, we believed that the de novo genome sequencing error should answer for the COMT gene in giant panda, which had 11 nucleotide deletions in the genome database. Although the COMT gene is intact in giant panda and red panda, the possibility that COMT is associated with their bamboo eating behavior can still not be ruled out. COMT gene codes an enzyme that plays a critical role in dopamine metabolic system. Recent papers showed that COMT was involved in appetite regulation (Galvao et al., 2012), bulimia nervosa (Groleau et al., 2012; Thaler et al., 2012), and anorexia nervosa in human (Brandys et al., 2012; Favaro et al., 2013). Our results demonstrated that the primary structure of COMT had not changed in giant panda and red panda, comparing with that from other species, which indicated that the primary structure of COMT was not the answer for giant panda's food choice. However, as previous study revealed that both the weaker Kozak motif of COMT and predicted miRNA binding sites of 3′UTR of COMT probably leaded to lower expression of COMT in giant panda (Jin et al., 2011). It is still possible that giant panda's bamboo eating behavior was affected by reducing expression of COMT. And further analysis on expression level of COMT is helpful for understanding its function in giant panda and red panda. In addition, some studies currently reported that gut microbiome may partially clarify the digestion of bamboo lignin in giant panda and red panda (Fang et al., 2012; Kong et al., 2014; Tun et al., 2014). Even then, what's the real driving force behind the giant panda's diet switch is still a mystery. Further investigation on the bamboo eating behavior of giant panda and red panda, the gut microbiome may be the research direction, which has a close relationship with food choices. Acknowledgments This work was supported by the “1000-Talent Program” in Sichuan, the Science Foundation for Youths of Sichuan Province (2013JQ0014), the National Natural Science Foundation of China (31471997) and the Innovative Research Team in University of Sichuan Bureau of Education (035z1060). Appendix A. Supplementary data
References Brandys, M.K., Landt, M.C.T.S.-O.T., van Elburg, A.A., Ophoff, R., Verduijn, W., Meulenbelt, I., Middeldorp, C.M., Boomsma, D.I., van Furth, E.F., Slagboom, E., Kas, M.J.H., Adan, R.A.H., 2012. Anorexia nervosa and the Val158Met polymorphism of the COMT gene: meta-analysis and new data. Psychiatr. Genet. 22, 130–136. Fang, W., Fang, Z., Zhou, P., Chang, F., Hong, Y., Zhang, X., Peng, H., Xiao, Y., 2012. Evidence for lignin oxidation by the giant panda fecal microbiome. PLoS One 7, e50312. Favaro, A., Clementi, M., Manara, R., Bosello, R., Forzan, M., Bruson, A., Tenconi, E., Degortes, D., Titton, F., Di Salle, F., Santonastaso, P., 2013. Catechol-O-methyltransferase genotype modifies executive functioning and prefrontal functional connectivity in women with anorexia nervosa. J. Psychiatry Neurosci. 38, 241–248. Galvao, A.C.S., Krueger, R.C., Campagnolo, P.D.B., Mattevi, V.S., Vitolo, M.R., Almeida, S., 2012. Association of MAOA and COMT gene polymorphisms with palatable food intake in children. J. Nutr. Biochem. 23, 272–277. Glatston, A.R., 2010. Red Panda: Biology and Conservation of the First Panda. William Andrew Publishing, Norwich, NY. Groleau, P., Steiger, H., Joober, R., Bruce, K.R., Israel, M., Badawi, G., Zeramdini, N., Sycz, L., 2012. Dopamine-system genes, childhood abuse, and clinical manifestations in women with bulimia-spectrum disorders. J. Psychiatr. Res. 46, 1139–1145. Huotari, M., Gogos, J.A., Karayiorgou, M., Koponen, O., Forsberg, M., Raasmaja, A., Hyttinen, J., Männistö, P.T., 2002. Brain catecholamine metabolism in catechol-Omethyltransferase (COMT)-deficient mice. Eur. J. Neurosci. 15, 246–256. Jin, C., Ciochon, R.L., Dong, W., Hunt, R.M., Liu, J., Jaeger, M., Zhu, Q., 2007. The first skull of the earliest giant panda. Proc. Natl. Acad. Sci. U. S. A. 104, 10932–10937. Jin, K., Xue, C., Wu, X., Qian, J., Zhu, Y., Yang, Z., Yonezawa, T., Crabbe, M.J.C., Cao, Y., Hasegawa, M., 2011. Why does the giant panda eat bamboo? A comparative analysis of appetite-reward-related genes among mammals. PLoS One 6, e22602. Kong, F., Zhao, J., Han, S., Zeng, B., Yang, J., Si, X., Yang, B., Yang, M., Xu, H., Li, Y., 2014. Characterization of the gut microbiota in the red panda (Ailurus fulgens). PLoS One 9, e87885. Kozukue, E., KOZUKUE, N., Kurosaki, T., 1983. Organic acid, sugar and amino acid composition of bamboo shoots. J. Food Sci. 48, 935–938. Li, R., Fan, W., Tian, G., Zhu, H., He, L., Cai, J., Huang, Q., Cai, Q., Li, B., Bai, Y., 2009. The sequence and de novo assembly of the giant panda genome. Nature 463, 311–317. Mikolajczyk, E., Grzywacz, A., Samochowiec, J., 2010. The association of catechol-Omethyltransferase genotype with the phenotype of women with eating disorders. Brain Res. 1307, 142–148. Nelson, G., Chandrashekar, J., Hoon, M.A., Feng, L., Zhao, G., Ryba, N.J., Zuker, C.S., 2002. An amino-acid taste receptor. Nature 416, 199–202. Rutherford, K., Le Trong, I., Stenkamp, R., Parson, W., 2008. Crystal structures of human 108 V and 108 M catechol O-methyltransferase. J. Mol. Biol. 380, 120–130. Thaler, L., Groleau, P., Badawi, G., Sycz, L., Zeramdini, N., Too, A., Israel, M., Joober, R., Bruce, K.R., Steiger, H., 2012. Epistatic interactions implicating dopaminergic genes in bulimia nervosa (BN): relationships to eating- and personality-related psychopathology. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 39, 120–128. Tun, H.M., Mauroo, N.F., San Yuen, C., Ho, J.C.W., Wong, M.T., Leung, F.C.-C., 2014. Microbial diversity and evidence of novel homoacetogens in the gut of both geriatric and adult giant pandas (Ailuropoda melanoleuca). PLoS One 9, e79902. Wise, R.A., 2004. Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483–494. Yilmaz, Z., Kaplan, A.S., Zai, C.C., Levitan, R.D., Kennedy, J.L., 2011. COMT Val158Met variant and functional haplotypes associated with childhood ADHD history in women with bulimia nervosa. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 35, 948–952. Zhao, H., Yang, J.-R., Xu, H., Zhang, J., 2010. Pseudogenization of the umami taste receptor gene Tas1r1 in the giant panda coincided with its dietary switch to bamboo. Mol. Biol. Evol. 27, 2669–2673.
Jingsi Tang1 Fanli Kong1 Bo Zeng Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural Universtiy, Chengdu 611130, China Huailiang Xu Jiandong Yang College of Animal Science and Technology, Sichuan Agricultural University, Ya'an, Sichuan, China Ying Li Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural Universtiy, Chengdu 611130, China Corresponding author. E-mail address: [email protected].
Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.gene.2015.02.046.
9 January 2015
1
These authors contributed equally to this work.
Contents lists available at ScienceDirect
Gene journal homepage: www.elsevier.com/locate/gene
Letter to the Editor The primary structure of COMT gene is not involved in the diet shift of the giant or the red pandas Keywords: COMT Diet shift Giant panda Red panda
Dear Editor, The giant panda (Ailuropoda melanoleuca) is an endangered species in China. As one species of family Ursidae order Carnivore, the giant panda has a very special bamboo diet, which is different from carnivores or omnivores of this order. That makes evolutionists so interested in the giant panda. Approximately 7 Ma ago, the ancient giant panda was still omnivorous (Jin et al., 2007). However, after 4.6 Ma to 5 Ma of evolution, the giant panda became herbivores and mainly feed on soft bamboo shoots, stems, and leaves (Jin et al., 2007). The modern giant panda consumes bamboos everyday, which account for 99% of its diet (Zhao et al., 2010). What's more, the giant panda also developed an enlarged radial sesamoid that functions as a thumb to grab bamboo (Jin et al., 2011). However, the giant panda possesses a more similar gastrointestinal tract type to those of carnivores than herbivores (Li et al., 2009). In other words, the digestive system of giant panda is more suitable for a meat diet than a bamboo diet. Worst of all, the giant panda lack the putative genes encoding for enzymes degrading lignocelluloses, which is the dominating component of bamboo (Li et al., 2009). Therefore, what is the real driving force that makes the giant panda diet switch is still an interesting question. Recently, several groups have attempted to characterize the cause of the giant panda diet switch. One of these groups reported that the T1R1 gene in the giant panda genome turned to be a pseudogene due to two frame-shifting mutations in exon 3 and exon 6, respectively (Li et al., 2009). T1R1 belongs to the vertebrate T1R family that comprises of three members in most species, and T1R1 and T1R3 form a heterodimer receptor that mediates the umami taste, which is the taste of glutamic acid and other amino acids (Nelson et al., 2002). But in bamboo amino acids level are less than in animal tissues (Kozukue et al., 1983). Thus another paper suggested that the lost function of T1R1 may result in the giant panda diet switch (Zhao et al., 2010). Furthermore, they found that T1R1 is intact in carnivores except giant panda. However, the T1R1 gene is also intact in some herbivorous such as cow and horse, which implies that the pseudogenization of T1R1 may not be the only reason for the giant panda eating bamboo.
Abbreviations: COMT, catechol-o-methyltransferase, T1R1, taste receptor type 1 member 1, T1R3, taste receptor type 1 member 3, SAM, S-adenosyl methionine.
http://dx.doi.org/10.1016/j.gene.2015.02.046 0378-1119/© 2015 Elsevier B.V. All rights reserved.
Another group proposed that the distinctive COMT is responsible for the giant panda's food choice by a comprehensive analysis (Jin et al., 2011). COMT is an enzyme that degrades catecholamines such as dopamine, epinephrine, and norepinephrine. The enzyme introduces a methyl group to the catecholamine, which is donated by the methionine portion of SAM. In human COMT, the methionine portion of SAM is fixed in the right place by hydrogen bonds with several vital residues in α3, α4, and β4 (Rutherford et al., 2008). Firstly, compared with other eight species, the predicted COMT protein appeared four amino acid deletions in giant panda, leading to an important change from the α4 helix to a more flexible loop in the panda's COMT structure (Jin et al., 2011). Such structural variation of the giant panda's COMT may have a relatively weak effect on inactivating catecholamines. Secondly, focusing on the Kozak consensus sequence, they observed that COMT in giant panda had a weaker Kozak motif (Jin et al., 2011). That may cause a lower expression of COMT, and probably can further enhance the effect of its coding region. Thirdly, in the post-transcription regulation level, the 3′UTR of COMT gene was predicted to be regulated by miR-199a-5p in giant panda but not in human (Jin et al., 2011). The predicted miRNA regulation may reduce the mRNA level of COMT. To some extent, it enhances the catecholamine level. Previous studies indicated that COMTdeficient male mice had promoted dopamine levels (Huotari et al., 2002), which could improve appetite in mice (Wise, 2004). And some papers found that several mutations of COMT were connected with eating disorders in human (Mikolajczyk et al., 2010; Yilmaz et al., 2011; Groleau et al., 2012; Favaro et al., 2013). Hence, it is very possible that the potential lower activity of COMT in giant panda is associated with its eating bamboo diet. Red panda (Ailurus fulgens) is the only living species of the genus Ailurus and the family Ailuridae. Like the giant panda, the red panda also regards the bamboo as its major food source, which occupies over 90% of its diet (Glatston, 2010). However, because its digestive system is relatively short and simple, the red panda also can't process bamboo well. Therefore, we hypothesized that the COMT may be related to the red panda diet switch, like giant panda. In this study, firstly, we collected one blood sample of giant panda (Giant panda 1) from the China Conservation and Research Center for the Giant Panda, Ya'an, Sichuan Province, China, and one muscle sample (Red panda 1) from a dead red panda found in the Fengtongzhai National Nature Reserve (Baoxing, Sichuan Province, China), both blood and tissue samples were stored at − 20 °C before use. DNA was extracted from these samples by using the TIANamp Genomic DNA Kit according to the manufacturer's protocol. Based on multiple sequence alignment of COMT coding region from nine mammals (Table S1), we designed one pair of specific primers (Table S2) for amplifying the interesting region of COMT gene. PCR products were then cloned into pEASY-T1 Simple Cloning vector. Two colonies for each sample were picked and their plasmids were sequenced by Invitrogen Company. Surprisingly, neither the giant panda nor the red panda showed a four amino acids' deletion in the COMT region (Fig. 1A), which was reported to have involved in the diet shift in giant panda (Jin et al., 2011). Based on our results, we supposed that the deletions may due to the polymorphism
Letter to the Editor
245
Giant panda
Fig. 1. COMT gene is intact both in giant panda and red panda. A: Alignment of the partial amino acids of COMT in nine species. Giant panda 1, Giant panda 2, Red panda 1, and Red panda 2 were sequenced by this study, all other sequences were downloaded from Ensemble. B: Comparison diagram of COMT gene in giant panda and dog. The red box refers to the coding exon and the white box stands for the intron. C: Alignment of the second coding exon in ten species. The sequence of giant panda (downloaded) was comprised of the second coding exon, the second intron, and the third coding exon.
246
Letter to the Editor
of the COMT among individuals of the giant and red pandas, or the genome sequencing error in the giant panda. To further determine if there are polymorphisms in COMT gene, we collected two fecal samples from giant panda (Giant panda 2) and red panda (Red panda 2), respectively. Another pair of specific primers (Table S2) was designed. DNA sequencing results showed that the COMT genes of giant panda and red panda both still possessed the four amino acids (Fig. 1A), which formed the important α4 helix. Therefore, the 4 amino acid deletion genotype of the COMT, if it exists, is not dominant, and thus can hardly explain the diet shift of the giant or red panda. While it's possible that the 12 nucleotides missing of the COMT in giant panda are artificial and caused by the genome sequencing mistake. The COMT gene in giant panda has five coding exons and four introns, but in dog' COMT there are only four coding exons and three introns (Fig. 1B). Moreover, the deletion happened between the second coding exon and the third coding exon in giant panda. And it was strange that the second intron of COMT gene only had a single A in giant panda genome. Thus we speculated that there was no intron between the second coding exon and the third coding exon. In other words, COMT has four coding exons in giant panda as well. To confirm this prediction, we compared the second coding exon of COMT gene of giant panda with that of other eight species. The result clearly showed that COMT gene indeed in giant panda had no difference with other species' COMT (Fig. 1C) in terms of the exon–intron structure. Hence, we believed that the de novo genome sequencing error should answer for the COMT gene in giant panda, which had 11 nucleotide deletions in the genome database. Although the COMT gene is intact in giant panda and red panda, the possibility that COMT is associated with their bamboo eating behavior can still not be ruled out. COMT gene codes an enzyme that plays a critical role in dopamine metabolic system. Recent papers showed that COMT was involved in appetite regulation (Galvao et al., 2012), bulimia nervosa (Groleau et al., 2012; Thaler et al., 2012), and anorexia nervosa in human (Brandys et al., 2012; Favaro et al., 2013). Our results demonstrated that the primary structure of COMT had not changed in giant panda and red panda, comparing with that from other species, which indicated that the primary structure of COMT was not the answer for giant panda's food choice. However, as previous study revealed that both the weaker Kozak motif of COMT and predicted miRNA binding sites of 3′UTR of COMT probably leaded to lower expression of COMT in giant panda (Jin et al., 2011). It is still possible that giant panda's bamboo eating behavior was affected by reducing expression of COMT. And further analysis on expression level of COMT is helpful for understanding its function in giant panda and red panda. In addition, some studies currently reported that gut microbiome may partially clarify the digestion of bamboo lignin in giant panda and red panda (Fang et al., 2012; Kong et al., 2014; Tun et al., 2014). Even then, what's the real driving force behind the giant panda's diet switch is still a mystery. Further investigation on the bamboo eating behavior of giant panda and red panda, the gut microbiome may be the research direction, which has a close relationship with food choices. Acknowledgments This work was supported by the “1000-Talent Program” in Sichuan, the Science Foundation for Youths of Sichuan Province (2013JQ0014), the National Natural Science Foundation of China (31471997) and the Innovative Research Team in University of Sichuan Bureau of Education (035z1060). Appendix A. Supplementary data
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Jingsi Tang1 Fanli Kong1 Bo Zeng Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural Universtiy, Chengdu 611130, China Huailiang Xu Jiandong Yang College of Animal Science and Technology, Sichuan Agricultural University, Ya'an, Sichuan, China Ying Li Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural Universtiy, Chengdu 611130, China Corresponding author. E-mail address: [email protected].
Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.gene.2015.02.046.
9 January 2015
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These authors contributed equally to this work.