Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage

Guang-Qi GAO; Li-Shuang SONG; Bin TONG; Guang-Peng LI

doi:10.13918/j.issn.2095-8137.2016.3.144

Volume 37 Issue 3

May 2016

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Guang-Qi GAO, Li-Shuang SONG, Bin TONG, Guang-Peng LI. Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage. Zoological Research, 2016, 37(3): 144-150. doi: 10.13918/j.issn.2095-8137.2016.3.144

Citation:

Guang-Qi GAO, Li-Shuang SONG, Bin TONG, Guang-Peng LI. Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage. Zoological Research, 2016, 37(3): 144-150. doi: 10.13918/j.issn.2095-8137.2016.3.144

Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage

doi: 10.13918/j.issn.2095-8137.2016.3.144

Research Center for Laboratory of Animal Science, Inner Mongolia University, Hohhot 010070, China

Funds: This work was supported by the 2014 Fundamental Research Program from Science and Technology of the Inner Mongolia Autonomous Region of China

More Information

Corresponding author: Guang-Peng LI
Received Date: 2016-01-05
Rev Recd Date: 2016-03-28
Publish Date: 2016-05-18

Abstract

Carotenoids, which generate yellow, orange, and red colors, are crucial pigments in avian plumage. Investigations into genes associated with carotenoidbased coloration in avian species are important; however, such research is difficult because carotenoids cannot be synthetized in vertebrates as they are only derived from dietary sources. Here, the golden pheasant (Chrysolophus pictus) was used as a model in analysis of candidate gene expression profiles implicated in carotenoid binding and deposition. Using mass and Raman spectrometry to confirm the presence of carotenoids in golden pheasant feathers, we found C₄₀H₅₄O and C₄₀H₅₆O₂ in feathers with yellow to red colors, and in the rachis of iridescent feathers. The global gene expression profiles in golden pheasant skins were analyzed by RNA-seq and all six carotenoid binding candidate genes sequenced were studied by realtime PCR. StAR4, GSTA2, Scarb1, and APOD in feather follicles showed different expressions in red breast and orange nape feathers compared with that of iridescent mantle feathers. Further comparison of golden pheasant yellow rump and Lady Amherst's pheasant (Chrysolophus amherstiae) white nape feathers suggested that GSTA2 and APOD played a potential role in carotenoid-based coloration in golden pheasant.
- Expression,
- Carotenoid coloration,
- Candidate genes,
- Golden pheasant,
- Feather

References

[1]	Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Annals of Statistics, 29(4):1165-1188.
[2]	Bhosale P, Li BX, Sharifzadeh M, Gellermann W, Frederick JM, Tsuchida K, Bernstein PS. 2009. Purification and partial characterization of a luteinbinding protein from human retina. Biochemistry, 48(22):4798-4807.
[3]	During A, Doraiswamy S, Harrison EH. 2008. Xanthophylls are preferentially taken up compared with β-carotene by retinal cells via a SRBIdependent mechanism. Journal of Lipid Research, 49(8):1715-1724.
[4]	Eriksson J, Larson G, Gunnarsson U, Bed'hom B, Tixier-Boichard M, Strömstedt L, Wright D, Jungerius A, Vereijken A, Randi E, Jensen P, Andersson L. 2008. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genetics, 4(2):e1000010.
[5]	Galván I, Jorge A, Ito K, Tabuchi K, Solano F, Wakamatsu K. 2013. Raman spectroscopy as a non-invasive technique for the quantification of melanins in feathers and hairs. Pigment Cell & Melanoma Research, 26(6):917-923.
[6]	Ganfornina MD, Sánchez D, Pagano A, Tonachini L, Descalzi-Cancedda F, Martínez S. 2005. Molecular characterization and developmental expression pattern of the chicken apolipoprotein D gene:implications for the evolution of vertebrate lipocalins. Developmental Dynamics, 232(1):191-199.
[7]	Hill GE, McGraw KJ. 2006. Bird Coloration, vol. 1, Mechanisms and Measurements. Havard:Havard University Press, 177-242.
[8]	LaFountain AM, Kaligotla S, Cawley S, Riedl KM, Schwartz SJ, Frank HA, Prum RO. 2010. Novel methoxy-carotenoids from the burgundy-colored plumage of the Pompadour Cotinga Xipholena punicea. Archives of Biochemistry and Biophysics, 504(1):142-153.
[9]	McGraw KJ, Adkins-Regan E, Parker RS. 2002a. Anhydrolutein in the zebra finch:a new, metabolically derived carotenoid in birds. Comparative Biochemistry and Physiology Part B-Biochemistry & Molecular Biology, 132(4):811-818.
[10]	McGraw KJ, Hill GE, Stradi R, Parker RS. 2002b. The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch. Comparative Biochemistry and Physiology Part B-Biochemistry & Molecular Biology, 131(2):261-269.
[11]	McGraw KJ, Beebee MD, Hill GE, Parker RS. 2003. Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation in to feathers. Comparative Biochemistry and Physiology Part BBiochemistry & Molecular Biology, 135(4):689-696.
[12]	McGraw KJ, Hudon J, Hill GE, Parker RS. 2005. A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behavioral Ecology & Sociobiology, 57(4):391-397.
[13]	Mendes-Pinto MM, Lafountain AM, Stoddard MC, Prum RO, Frank HA, Robert B. 2012. Variation in carotenoid-protein interaction in bird feathers produces novel plumage coloration. Journal of the Royal Society Interface, 9(77):3338-3350.
[14]	Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5(7):621-628.
[15]	Poelstra JW, Vijay N, Bossu CM, Lantz H, Ryll B, Müller I, Baglione V, Unneberg P, Wikelski M, Grabherr MG, Wolf JBW. 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science, 344(6190):1410-1414.
[16]	Pointer MA, Prager M, Andersson S, Mundy NI. 2012. A novel method for screening a vertebrate transcriptome for genes involved in carotenoid binding and metabolism. Molecular Ecology Resources, 12(1):149-159.
[17]	Roulin A, Ducrest AL. 2013. Genetics of colouration in birds. Seminars in Cell & Developmental Biology, 24(6-7):594-608.
[18]	Stradi R, Celentano G, Rossi E, Rovati G, Pastore M. 1995. Carotenoids in bird plumage:I. The carotenoid pattern in a series of palearctic carduelinae. Comparative Biochemistry and Physiology Part B-Biochemistry and Molecular Biology, 110(1):131-143.
[19]	Thomas DB, McGraw KJ, Butler MW, Carrano MT, Madden O, James HF. 2014a. Ancient origins and multiple appearances of carotenoid-pigmented feathers in birds. Proceedings of the Royal Society B-Biological Sciences, 281(1788):20140806.
[20]	Thomas DB, McGraw KJ, James HF, Madden O. 2014b. Non-destructive descriptions of carotenoids in feathers using Raman spectroscopy. Analytical Methods, 6(5):1301-1308.
[21]	Walsh N, Dale J, McGraw KJ, Pointer MA Mundy NI. 2012. Candidate genes for carotenoid coloration in vertebrates and their expression profiles in the carotenoid-containing plumage and bill of a wild bird. Proceedings of the Royal Society B-Biological Sciences, 279(1726):58-66.
[22]	Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu LH, Pan HL, Wang ZJ, Jin LJ, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang ZK, Liu Y, Xie QL, Yu H, Lian JM, Wen P, Zhang F, Li H, Zeng YL, Xiong ZJ, Liu SP, Zhou L, Huang ZY, An N, Wang J, Zheng QM, Xiong YQ, Wang GB, Wang B, Wang JJ, Fan Y, da Fonseca RR, Alfaro-Núñez A, Schubert M, Orlando L, Mourier T, Howard JT, Ganapathy G, Pfenning A, Whitney O, Rivas MV, Hara E, Smith J, Farré M, Narayan J, Slavov G, Romanov MN, Borges R, Machado JP, Khan I, Springer MS, Gatesy J, Hoffmann FG, Opazo JC, Håstad O, Sawyer RH, Kim H, Kim KW, Kim HJ, Cho S, Li N, Huang Y, Bruford MW, Zhan XJ, Dixon A, Bertelsen MF, Derryberry E, Warren W, Wilson RK, Li SB, Ray DA, Green RE, O'Brien SJ, Griffin D, Johnson WE, Haussler D, Ryder OA, Willerslev E, Graves GR, Alström P, Fjeldså J, Mindell DP, Edwards SV, Braun EL, Rahbek C, Burt DW, Houde P, Zhang Y, Yang HM, Wang J; Avian Genome Consortium, Jarvis ED, Gilbert MTP, Wang J. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215):1311-1320.

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通讯作者: 陈斌, bchen63@163.com

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沈阳化工大学材料科学与工程学院沈阳 110142

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Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage

Research Center for Laboratory of Animal Science, Inner Mongolia University, Hohhot 010070, China

Funds: This work was supported by the 2014 Fundamental Research Program from Science and Technology of the Inner Mongolia Autonomous Region of China

Corresponding author: Guang-Peng LI

Received Date: 2016-01-05

Rev Recd Date: 2016-03-28

Publish Date: 2016-05-18

Key words:

Abstract: Carotenoids, which generate yellow, orange, and red colors, are crucial pigments in avian plumage. Investigations into genes associated with carotenoidbased coloration in avian species are important; however, such research is difficult because carotenoids cannot be synthetized in vertebrates as they are only derived from dietary sources. Here, the golden pheasant (Chrysolophus pictus) was used as a model in analysis of candidate gene expression profiles implicated in carotenoid binding and deposition. Using mass and Raman spectrometry to confirm the presence of carotenoids in golden pheasant feathers, we found C₄₀H₅₄O and C₄₀H₅₆O₂ in feathers with yellow to red colors, and in the rachis of iridescent feathers. The global gene expression profiles in golden pheasant skins were analyzed by RNA-seq and all six carotenoid binding candidate genes sequenced were studied by realtime PCR. StAR4, GSTA2, Scarb1, and APOD in feather follicles showed different expressions in red breast and orange nape feathers compared with that of iridescent mantle feathers. Further comparison of golden pheasant yellow rump and Lady Amherst's pheasant (Chrysolophus amherstiae) white nape feathers suggested that GSTA2 and APOD played a potential role in carotenoid-based coloration in golden pheasant.

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Reference (22)

[1]	Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Annals of Statistics, 29(4):1165-1188.
[2]	Bhosale P, Li BX, Sharifzadeh M, Gellermann W, Frederick JM, Tsuchida K, Bernstein PS. 2009. Purification and partial characterization of a luteinbinding protein from human retina. Biochemistry, 48(22):4798-4807.
[3]	During A, Doraiswamy S, Harrison EH. 2008. Xanthophylls are preferentially taken up compared with β-carotene by retinal cells via a SRBIdependent mechanism. Journal of Lipid Research, 49(8):1715-1724.
[4]	Eriksson J, Larson G, Gunnarsson U, Bed'hom B, Tixier-Boichard M, Strömstedt L, Wright D, Jungerius A, Vereijken A, Randi E, Jensen P, Andersson L. 2008. Identification of the yellow skin gene reveals a hybrid origin of the domestic chicken. PLoS Genetics, 4(2):e1000010.
[5]	Galván I, Jorge A, Ito K, Tabuchi K, Solano F, Wakamatsu K. 2013. Raman spectroscopy as a non-invasive technique for the quantification of melanins in feathers and hairs. Pigment Cell & Melanoma Research, 26(6):917-923.
[6]	Ganfornina MD, Sánchez D, Pagano A, Tonachini L, Descalzi-Cancedda F, Martínez S. 2005. Molecular characterization and developmental expression pattern of the chicken apolipoprotein D gene:implications for the evolution of vertebrate lipocalins. Developmental Dynamics, 232(1):191-199.
[7]	Hill GE, McGraw KJ. 2006. Bird Coloration, vol. 1, Mechanisms and Measurements. Havard:Havard University Press, 177-242.
[8]	LaFountain AM, Kaligotla S, Cawley S, Riedl KM, Schwartz SJ, Frank HA, Prum RO. 2010. Novel methoxy-carotenoids from the burgundy-colored plumage of the Pompadour Cotinga Xipholena punicea. Archives of Biochemistry and Biophysics, 504(1):142-153.
[9]	McGraw KJ, Adkins-Regan E, Parker RS. 2002a. Anhydrolutein in the zebra finch:a new, metabolically derived carotenoid in birds. Comparative Biochemistry and Physiology Part B-Biochemistry & Molecular Biology, 132(4):811-818.
[10]	McGraw KJ, Hill GE, Stradi R, Parker RS. 2002b. The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch. Comparative Biochemistry and Physiology Part B-Biochemistry & Molecular Biology, 131(2):261-269.
[11]	McGraw KJ, Beebee MD, Hill GE, Parker RS. 2003. Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation in to feathers. Comparative Biochemistry and Physiology Part BBiochemistry & Molecular Biology, 135(4):689-696.
[12]	McGraw KJ, Hudon J, Hill GE, Parker RS. 2005. A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behavioral Ecology & Sociobiology, 57(4):391-397.
[13]	Mendes-Pinto MM, Lafountain AM, Stoddard MC, Prum RO, Frank HA, Robert B. 2012. Variation in carotenoid-protein interaction in bird feathers produces novel plumage coloration. Journal of the Royal Society Interface, 9(77):3338-3350.
[14]	Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods, 5(7):621-628.
[15]	Poelstra JW, Vijay N, Bossu CM, Lantz H, Ryll B, Müller I, Baglione V, Unneberg P, Wikelski M, Grabherr MG, Wolf JBW. 2014. The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science, 344(6190):1410-1414.
[16]	Pointer MA, Prager M, Andersson S, Mundy NI. 2012. A novel method for screening a vertebrate transcriptome for genes involved in carotenoid binding and metabolism. Molecular Ecology Resources, 12(1):149-159.
[17]	Roulin A, Ducrest AL. 2013. Genetics of colouration in birds. Seminars in Cell & Developmental Biology, 24(6-7):594-608.
[18]	Stradi R, Celentano G, Rossi E, Rovati G, Pastore M. 1995. Carotenoids in bird plumage:I. The carotenoid pattern in a series of palearctic carduelinae. Comparative Biochemistry and Physiology Part B-Biochemistry and Molecular Biology, 110(1):131-143.
[19]	Thomas DB, McGraw KJ, Butler MW, Carrano MT, Madden O, James HF. 2014a. Ancient origins and multiple appearances of carotenoid-pigmented feathers in birds. Proceedings of the Royal Society B-Biological Sciences, 281(1788):20140806.
[20]	Thomas DB, McGraw KJ, James HF, Madden O. 2014b. Non-destructive descriptions of carotenoids in feathers using Raman spectroscopy. Analytical Methods, 6(5):1301-1308.
[21]	Walsh N, Dale J, McGraw KJ, Pointer MA Mundy NI. 2012. Candidate genes for carotenoid coloration in vertebrates and their expression profiles in the carotenoid-containing plumage and bill of a wild bird. Proceedings of the Royal Society B-Biological Sciences, 279(1726):58-66.
[22]	Zhang GJ, Li C, Li QY, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu LH, Pan HL, Wang ZJ, Jin LJ, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang ZK, Liu Y, Xie QL, Yu H, Lian JM, Wen P, Zhang F, Li H, Zeng YL, Xiong ZJ, Liu SP, Zhou L, Huang ZY, An N, Wang J, Zheng QM, Xiong YQ, Wang GB, Wang B, Wang JJ, Fan Y, da Fonseca RR, Alfaro-Núñez A, Schubert M, Orlando L, Mourier T, Howard JT, Ganapathy G, Pfenning A, Whitney O, Rivas MV, Hara E, Smith J, Farré M, Narayan J, Slavov G, Romanov MN, Borges R, Machado JP, Khan I, Springer MS, Gatesy J, Hoffmann FG, Opazo JC, Håstad O, Sawyer RH, Kim H, Kim KW, Kim HJ, Cho S, Li N, Huang Y, Bruford MW, Zhan XJ, Dixon A, Bertelsen MF, Derryberry E, Warren W, Wilson RK, Li SB, Ray DA, Green RE, O'Brien SJ, Griffin D, Johnson WE, Haussler D, Ryder OA, Willerslev E, Graves GR, Alström P, Fjeldså J, Mindell DP, Edwards SV, Braun EL, Rahbek C, Burt DW, Houde P, Zhang Y, Yang HM, Wang J; Avian Genome Consortium, Jarvis ED, Gilbert MTP, Wang J. 2014. Comparative genomics reveals insights into avian genome evolution and adaptation. Science, 346(6215):1311-1320.

Expression levels of GSTA2 and APOD genes might be associated with carotenoid coloration in golden pheasant (Chrysolophus pictus) plumage

doi: 10.13918/j.issn.2095-8137.2016.3.144

Abstract

References

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通讯作者: 陈斌, bchen63@163.com

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