Whole genome sequencing identifies candidate genes and mutations that can explain diluted and other colour varieties of domestic canaries (Serinus canaria).
MLPH
SNP
avian species
breeding
domestication
feather colour
indel
mutation
pigmentation
songbird
Journal
Animal genetics
ISSN: 1365-2052
Titre abrégé: Anim Genet
Pays: England
ID NLM: 8605704
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
revised:
07
03
2023
received:
07
03
2023
accepted:
03
05
2023
medline:
6
7
2023
pubmed:
17
5
2023
entrez:
17
5
2023
Statut:
ppublish
Résumé
The domestic canary (Serinus canaria) is one of the most common pet birds and has been extensively selected and bred over the last few centuries to constitute many different varieties. Plumage pigmentation is one of the main phenotypic traits that distinguish canary breeds and lines. Feather colours in these birds, similarly to other avian species, are mainly depended on the presence of two major types of pigments: carotenoids and melanins. In this study, we exploited whole genome sequencing (WGS) datasets produced from five canary lines or populations (Black Frosted Yellow, Opal, Onyx, Opal × Onyx and Mogno, some of which carrying different putative dilute alleles), complemented with other WGS datasets retrieved from previous studies, to identify candidate genes that might explain pigmentation variability across canary breeds and varieties. Sequencing data were obtained using a DNA pool-seq approach and genomic data were compared using window-based F
Substances chimiques
Carotenoids
36-88-4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
510-525Subventions
Organisme : Federazione Ornicoltori Italiani
Organisme : Università di Bologna
Informations de copyright
© 2023 The Authors. Animal Genetics published by John Wiley & Sons Ltd on behalf of Stichting International Foundation for Animal Genetics.
Références
Babovic, D., O'Tuathaigh, C.M., O'Connor, A.M., O'Sullivan, G.J., Tighe, O., Croke, D.T. et al. (2008) Phenotypic characterization of cognition and social behavior in mice with heterozygous versus homozygous deletion of catechol-O-methyltransferase. Neuroscience, 155, 1021-1029. Available from: https://doi.org/10.1016/j.neuroscience.2008.07.006
Baxter, L.L., Watkins-Chow, D.E., Pavan, W.J. & Loftus, S.K. (2019) A curated gene list for expanding the horizons of pigmentation biology. Pigment Cell & Melanoma Research, 32, 348-358. Available from: https://doi.org/10.1111/pcmr.12743
Bed'hom, B., Vaez, M., Coville, J.L., Gourichon, D., Chastel, O., Follett, S. et al. (2012) The lavender plumage colour in Japanese quail is associated with a complex mutation in the region of MLPH that is related to differences in growth, feed consumption and body temperature. BMC Genomics, 13, 442. Available from: https://doi.org/10.1186/1471-2164-13-442
Birkhead, T.R., Schulze-Hagen, K. & Kinzelbach, R. (2004) Domestication of the canary, Serinus canaria - the change from green to yellow. Archives of Natural History, 31, 50-56. Available from: https://doi.org/10.3366/anh.2004.31.1.50
Bovo, S., Ribani, A., Muñoz, M., Alves, E., Araujo, J.P., Bozzi, R. et al. (2020) Whole-genome sequencing of European autochthonous and commercial pig breeds allows the detection of signatures of selection for adaptation of genetic resources to different breeding and production systems. Genetics Selection Evolution, 52, 33. Available from: https://doi.org/10.1186/s12711-020-00553-7
Brush, A.H. (1990) Metabolism of carotenoid pigments in birds. FASEB Journal, 4, 2969-2977. Available from: https://doi.org/10.1096/fasebj.4.12.2394316
Campagna, L., Mo, Z., Siepel, A. & Uy, J.A.C. (2022) Selective sweeps on different pigmentation genes mediate convergent evolution of Island melanism in two incipient bird species. PLoS Genetics, 18, e1010474. Available from: https://doi.org/10.1371/journal.pgen.1010474
Deem, J.D., Faber, C.L. & Morton, G.J. (2022) AgRP neurons: regulators of feeding, energy expenditure, and behavior. The FEBS Journal, 289, 2362-2381. Available from: https://doi.org/10.1111/febs.16176
Denecker, G., Vandamme, N., Akay, O., Koludrovic, D., Taminau, J., Lemeire, K. et al. (2014) Identification of a ZEB2-MITF-ZEB1 transcriptional network that controls melanogenesis and melanoma progression. Cell Death and Differentiation, 21, 1250-1261. Available from: https://doi.org/10.1038/cdd.2014.44
Domyan, E.T., Guernsey, M.W., Kronenberg, Z., Krishnan, S., Boissy, R.E., Vickrey, A.I. et al. (2014) Epistatic and combinatorial effects of pigmentary gene mutations in the domestic pigeon. Current Biology, 24, 459-464. Available from: https://doi.org/10.1016/j.cub.2014.01.020c
Fontanesi, L., Forestier, L., Allain, D., Scotti, E., Beretti, F., Deretz-Picoulet, S. et al. (2010) Characterization of the rabbit agouti signaling protein (ASIP) gene: transcripts and phylogenetic analyses and identification of the causative mutation of the nonagouti black coat colour. Genomics, 95, 166-175. Available from: https://doi.org/10.1016/j.ygeno.2009.11.003
Fontanesi, L., Scotti, E., Allain, D. & Dall'Olio, S. (2014) A frameshift mutation in the melanophilin gene causes the dilute coat colour in rabbit (Oryctolagus cuniculus) breeds. Animal Genetics, 45, 248-255. Available from: https://doi.org/10.1111/age.12104
Gazda, M.A., Araújo, P.M., Lopes, R.J., Toomey, M.B., Andrade, P., Afonso, S. et al. (2020a) A genetic mechanism for sexual dichromatism in birds. Science, 368, 1270-1274. Available from: https://doi.org/10.1126/science.aba0803
Gazda, M.A., Toomey, M.B., Araújo, P.M., Lopes, R.J., Afonso, S., Myers, C.A. et al. (2020b) Genetic basis of de novo appearance of carotenoid ornamentation in bare parts of canaries. Molecular Biology and Evolution, 37, 1317-1328. Available from: https://doi.org/10.1093/molbev/msaa006
Gluckman, T.L. & Mundy, N.I. (2017) The differential expression of MC1R regulators in dorsal and ventral quail plumages during embryogenesis: implications for plumage pattern formation. PLoS One, 12, e0174714. Available from: https://doi.org/10.1371/journal.pone.0174714
Gunnarsson, U., Hellström, A.R., Tixier-Boichard, M., Minvielle, F., Bed'hom, B., Ito, S. et al. (2007) Mutations in SLC45A2 cause plumage color variation in chicken and Japanese quail. Genetics, 175, 867-877. Available from: https://doi.org/10.1534/genetics.106.063107
Hieu, H.T., Tanaka, M., Kuwamura, M., Mashimo, T., Serikawa, T. & Kuramoto, T. (2022) The rat Downunder (Du) coat color mutation is associated with eye anomalies and embryonic lethality and maps to a 3.9-mb region on chromosome 3. Experimental Animals, 72, 88-94. Available from: https://doi.org/10.1538/expanim.22-0086
Hiragaki, T., Inoue-Murayama, M., Miwa, M., Fujiwara, A., Mizutani, M., Minvielle, F. et al. (2008) Recessive black is allelic to the yellow plumage locus in Japanese quail and associated with a frameshift deletion in the ASIP gene. Genetics, 178, 771-775. Available from: https://doi.org/10.1534/genetics.107.077040
Ishida, Y., David, V.A., Eizirik, E., Schäffer, A.A., Neelam, B.A., Roelke, M.E. et al. (2006) A homozygous single-base deletion in MLPH causes the dilute coat color phenotype in the domestic cat. Genomics, 88, 698-705. Available from: https://doi.org/10.1016/j.ygeno.2006.06.006
Jeong, W., Bae, H., Lim, W., Bazer, F.W. & Song, G. (2017) Differential expression of neuregulin 1 (NRG1) and candidate miRNA regulating NRG1 transcription in the chicken oviduct in response to hormonal changes. Journal of Animal Science, 95, 3885-3904. Available from: https://doi.org/10.2527/jas2017.1663
Karlsson, E.K., Baranowska, I., Wade, C.M., Salmon Hillbertz, N.H., Zody, M.C., Anderson, N. et al. (2007) Efficient mapping of mendelian traits in dogs through genome-wide association. Nature Genetics, 39, 1321-1328. Available from: https://doi.org/10.1038/ng.2007.10
Kinoshita, K., Akiyama, T., Mizutani, M., Shinomiya, A., Ishikawa, A., Younis, H.H. et al. (2014) Endothelin receptor B2 (EDNRB2) is responsible for the tyrosinase-independent recessive white (mow) and mottled (mo) plumage phenotypes in the chicken. PLoS One, 9, e86361. Available from: https://doi.org/10.1371/journal.pone.0086361
Kondo, T. & Hearing, V.J. (2011) Update on the regulation of mammalian melanocyte function and skin pigmentation. Expert Review of Dermatology, 6, 97-108. Available from: https://doi.org/10.1586/edm.10.70
Lamorux, M.L., Delmas, V., Larue, L. & Bennett, D.C. (2010) The colors of mice: a model genetic network. Oxford, UK: Wiley-Blackwell.
Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics, 25, 1754-1760. Available from: https://doi.org/10.1093/bioinformatics/btp324
Li, L., Li, D., Liu, L., Li, S., Feng, Y., Peng, X. et al. (2015) Endothelin receptor B2 (EDNRB2) gene is associated with spot plumage pattern in domestic ducks (Anas platyrhynchos). PLoS One, 10, e0125883. Available from: https://doi.org/10.1371/journal.pone.0125883
Li, W., Sartelet, A., Tamma, N., Coppieters, W., Georges, M. & Charlier, C. (2016) Reverse genetic screen for loss-of-function mutations uncovers a frameshifting deletion in the melanophilin gene accountable for a distinctive coat color in Belgian blue cattle. Animal Genetics, 47, 110-113. Available from: https://doi.org/10.1111/age.12383
Li, J., Bed'hom, B., Marthey, S., Valade, M., Dureux, A., Moroldo, M. et al. (2019) A missense mutation in TYRP1 causes the chocolate plumage color in chicken and alters melanosome structure. Pigment Cell & Melanoma Research, 32, 381-390. Available from: https://doi.org/10.1111/pcmr.12753
Liu, H., Wang, J., Hu, J., Wang, L., Guo, Z., Fan, W. et al. (2022) Genome-wide association analysis reveal the genetic reasons affect melanin spot accumulation in beak skin of ducks. BMC Genomics, 23, 236. Available from: https://doi.org/10.1186/s12864-022-08444-5
Lopes, R.J., Johnson, J.D., Toomey, M.B., Ferreira, M.S., Araujo, P.M., Melo-Ferreira, J. et al. (2016) Genetic basis for red coloration in birds. Current Biology, 26, 1427-1434. Available from: https://doi.org/10.1016/j.cub.2016.03.076
Matesic, L.E., Yip, R., Reuss, A.E., Swing, D.A., O'Sullivan, T.N., Fletcher, C.F. et al. (2001) Mutations in Mlph, encoding a member of the Rab effector family, cause the melanosome transport defects observed in leaden mice. Proceedings of the National Academy of Sciences of the USA, 98, 10238-10243. Available from: https://doi.org/10.1073/pnas.181336698
McGraw, K.J. (2006) Mechanics of carotenoid-based coloration. In: Hill, G.E. & McGraw, K.J. (Eds.) Bird coloration. I. Mechanisms and measurements. Cambridge, MA, USA: Harvard University Press, pp. 177-242.
McLaren, W., Gil, L., Hunt, S.E., Riat, H.S., Ritchie, G.R., Thormann, A. et al. (2016) The Ensembl variant effect predictor. Genome Biology, 17, 122. Available from: https://doi.org/10.1186/s13059-016-0974-4
Miwa, M., Inoue-Murayama, M., Aoki, H., Kunisada, T., Hiragaki, T., Mizutani, M. et al. (2007) Endothelin receptor B2 (EDNRB2) is associated with the panda plumage colour mutation in Japanese quail. Animal Genetics, 38, 103-108. Available from: https://doi.org/10.1111/j.1365-2052.2007.01568.x
Nadeau, N.J., Mundy, N.I., Gourichon, D. & Minvielle, F. (2007) Association of a single-nucleotide substitution in TYRP1 with roux in Japanese quail (Coturnix japonica). Animal Genetics, 38, 609-613. Available from: https://doi.org/10.1111/j.1365-2052.2007.01667.x
Nadeau, N.J., Minvielle, F., Ito, S., Inoue-Murayama, M., Gourichon, D., Follett, S.A. et al. (2008) Characterization of Japanese quail yellow as a genomic deletion upstream of the avian homolog of the mammalian ASIP (agouti) gene. Genetics, 178, 777-786. Available from: https://doi.org/10.1534/genetics.107.077073
Nijenhuis, W.A.J., Oosterom, J. & Adan, R.A.H. (2001) AgRP (83-132) acts as an inverse agonist on the human-melanocortin-4 receptor. Molecular Endocrinology, 15, 164-171. Available from: https://doi.org/10.1210/mend.15.1.0578
Oribe, E., Fukao, A., Yoshihara, C., Mendori, M., Rosal, K.G., Takahashi, S. et al. (2012) Conserved distal promoter of the agouti signaling protein (ASIP) gene controls sexual dichromatism in chickens. General and Comparative Endocrinology, 177, 231-237. Available from: https://doi.org/10.1016/j.ygcen.2012.04.016
Parsons, J.J. (1987) The origin and dispersal of the domesticated canary. Journal of Cultural Geography, 7, 19-33. Available from: https://doi.org/10.1080/08873638709478505
Perez-Beato, O. (2008) Fundamentals of color genetics in canaries. Pittsburgh, Pennsylvania, USA: RoseDog Books.
Philipp, U., Hamann, H., Mecklenburg, L., Nishino, S., Mignot, E., Günzel-Apel, A.R. et al. (2005) Polymorphisms within the canine MLPH gene are associated with dilute coat color in dogs. BMC Genetics, 6, 34. Available from: https://doi.org/10.1186/1471-2156-6-34
Poplin, R., Ruano-Rubio, V., DePristo, M.A., Fennell, T.J., Carneiro, M.O., Van der Auwera, G.A. et al. (2017) Scaling accurate genetic variant discovery to tens of thousands of samples. bioRxiv, 201178. Available from: https://doi.org/10.1101/201178
Quinlan, A.R. & Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841-842. Available from: https://doi.org/10.1093/bioinformatics/btq033
R Core Team. (2018) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available from: http://www.R-project.org/
Ren, S., Lyu, G., Irwin, D.M., Liu, X., Feng, C., Luo, R. et al. (2021) Pooled sequencing analysis of geese (Anser cygnoides) reveals genomic variations associated with feather color. Frontiers in Genetics, 12, 650013. Available from: https://doi.org/10.3389/fgene.2021.650013
Robic, A., Morisson, M., Leroux, S., Gourichon, D., Vignal, A., Thebault, N. et al. (2019) Two new structural mutations in the 5′ region of the ASIP gene cause diluted feather color phenotypes in Japanese quail. Genetics Selection Evolution, 51, 12. Available from: https://doi.org/10.1186/s12711-019-0458-6
Rodríguez-Martínez, S. & Galván, I. (2020) A source of exogenous oxidative stress improves oxidative status and favors pheomelanin synthesis in zebra finches. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 228, 108667. Available from: https://doi.org/10.1016/j.cbpc.2019.108667
Schlötterer, C., Tobler, R., Kofler, R. & Nolte, V. (2014) Sequencing pools of individuals - mining genome-wide polymorphism data without big funding. Nature Reviews. Genetics, 15, 749-763. Available from: https://doi.org/10.1038/nrg3803
Stryjewski, K.F. & Sorenson, M.D. (2017) Mosaic genome evolution in a recent and rapid avian radiation. Nature Ecology & Evolution, 1, 1912-1922. Available from: https://doi.org/10.1038/s41559-017-0364-7
Sultana, H., Seo, D., Choi, N.R., Bhuiyan, M.S.A., Lee, S.H., Heo, K.N. et al. (2018) Identification of polymorphisms in MITF and DCT genes and their associations with plumage colors in Asian duck breeds. Asian-Australasian Journal of Animal Sciences, 31, 180-188. Available from: https://doi.org/10.5713/ajas.17.0298
Tang, H. & Thomas, P.D. (2016) PANTHER-PSEP: predicting disease-causing genetic variants using position-specific evolutionary preservation. Bioinformatics, 32, 2230-2232. Available from: https://doi.org/10.1093/bioinformatics/btw222
Toews, D.P., Taylor, S.A., Vallender, R., Brelsford, A., Butcher, B.G., Messer, P.W. et al. (2016) Plumage genes and little else distinguish the genomes of hybridizing warblers. Current Biology, 26, 2313-2318. Available from: https://doi.org/10.1016/j.cub.2016.06.034
Toomey, M.B., Lopes, R.J., Araújo, P.M., Johnson, J.D., Gazda, M.A., Afonso, S. et al. (2017) High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds. Proceedings of the National Academy of Sciences of the USA, 114, 5219-5224. Available from: https://doi.org/10.1073/pnas.1700751114
Toomey, M.B., Marques, C.I., Araújo, P.M., Huang, D., Zhong, S., Liu, Y. et al. (2022) A mechanism for red coloration in vertebrates. Current Biology, 32, 4201-4214.e12. Available from: https://doi.org/10.1016/j.cub.2022.08.013
Trigo, B.B., Utsunomiya, A.T.H., Fortunato, A.A.A.D., Milanesi, M., Torrecilha, R.B.P., Lamb, H. et al. (2021) Variants at the ASIP locus contribute to coat color darkening in Nellore cattle. Genetics Selectin Evolution, 53, 40. Available from: https://doi.org/10.1186/s12711-021-00633-2
Vaez, M., Follett, S.A., Bed'Hom, B., Gourichon, D., Tixier-Boichard, M. & Burke, T. (2008) A single point-mutation within the melanophilin gene causes the lavender plumage colour dilution phenotype in the chicken. BMC Genetics, 9, 7. Available from: https://doi.org/10.1186/1471-2156-9-7
Van Gele, M., Dynoodt, P. & Lambert, J. (2009) Griscelli syndrome: a model system to study vesicular trafficking. Pigment Cell & Melanoma Research, 22, 268-282. Available from: https://doi.org/10.1111/j.1755-148X.2009.00558.x
Vrieling, H., Duhl, D.M., Milla, S.E., Miller, K.A. & Barsh, G.S. (1994) Differences in dorsal and ventral pigmentation result from regional expression of the mouse agouti gene. Proceedings of the National Academy of Sciences of the USA, 91, 5667-5671. Available from: https://doi.org/10.1073/pnas.91.12.5667
Wang, Q., Pi, J., Pan, A., Shen, J. & Qu, L. (2017) A novel sex-linked mutant affecting tail formation in Hongshan chicken. Scientific Reports, 7, 10079. Available from: https://doi.org/10.1038/s41598-017-10943-5
Xi, Y., Wang, L., Liu, H., Ma, S., Li, Y., Li, L. et al. (2020) A 14-bp insertion in endothelin receptor B-like (EDNRB2) is associated with white plumage in Chinese geese. BMC Genomics, 21, 162. Available from: https://doi.org/10.1186/s12864-020-6562-8