Transcriptome analysis of feather follicles reveals candidate genes and pathways associated with pheomelanin pigmentation in chickens

Abstract

Yellow plumage is common in chickens, especially in breeds such as the Huiyang Bearded chicken, which is indigenous to China. We evaluated plumage colour distribution in F1, F2, and F3 populations of an Huiyang Bearded chicken × White Leghorn chicken cross, the heredity of the yellow plumage trait was distinguished from that of the gold plumage and other known plumage colours. Microscopic analysis of the feather follicles indicated that pheomelanin particles were formed in yellow but not in white feathers. to screen genes related to formation of the pheomelanin particles, we generated transcriptome data from yellow and white feather follicles from 7-and 11-week-old F3 chickens using RNA-seq. We identified 27 differentially expressed genes (DEGs) when comparing the yellow and white feather follicles. These DEGs were enriched in the Gene Ontology classes 'melanosome' and 'melanosome organization' related to the pigmentation process. Down-regulation of TYRP1, DCT, PMEL, MLANA, and HPGDS, verified using quantitative reverse transcription PCR, may lead to reduced eumelanin and increased pheomelanin synthesis in yellow plumage. owing to the presence of the Dominant white locus, both white and yellow plumage lack eumelanin, and white feathers showed no pigments. our results provide an understanding of yellow plumage formation in chickens. Plumage colour in birds, coat colour in mammals, and skin colour in humans have long been the focus of pigment research. Among these, birds display the most fascinating and complex colouration, which has been shown to be caused by melanin (eumelanin and pheomelanin), carotenoids, porphyrins, polyenes and structural colours 1,2. In general, the formation of different plumage colours in chickens is mainly attributed to variations in the quantity, proportion and location of eumelanin and pheomelanin in the feather 3. Eumelanin makes plumage appear black and dark brown, whereas pheomelanin makes it appear red and yellow 4. Both eumelanin and pheomelanin are indole-polymers with tyrosine as a precursor 5. During eumelanin synthesis, tyrosinase (TYR) catalyses the hydroxylation of tyrosine to 3,4-dihydroxyphenylalanine (dopa) and the oxidation of dopa to dopaquinone, which is then oxidized to form eumelanin; this occurs via the TYR family, involving TYR, tyrosinase-related protein 1 (TYRP1), and dopachrome tautomerase (DCT). Dopaquinone is transformed into 5-S-cysteinyldopa when cysteine or glutathione provides sulfhydryl; it eventually forms pheomelanin 5. In recent decades, with the rapid development of sequencing technology, significant progress has been made in the study of functional genes related to plumage colour in chickens. Various plumage colour causal genes, such as the Dominant white gene (I), recessive white gene (c), Silver gene (S), molted gene (mo) and Sex-linked barring gene (B), have been cloned 6-11. Especially for Dominant white allele (I), a strong dilutor of eumelanin owing to an insertion in the transmembrane region of the premelanosome protein (PMEL), it has no effect...

New insights into genetics underlying of plumage color

“…The significant interaction of the hematopoietic prostaglandin D synthase (HPGDS) gene in chromosome 3 with the GNG13 gene in chromosome 10 associated with plumage coloration has been revealed in our study. Also, down-regulation of HPGDS was displayed by transcriptome analysis, confirming its association with pheomelanin pigmentation in chickens with yellow plumage (Zheng et al 2020). Also, recently, Fogelholm et al (2020) reported five new candidate genes -CREBBP, WDR24, ARL8A, PHLDA3 and LAD1with putative small trans-acting effects by a combination of QTL mapping and a targeted genetic-genomics approach for plumage color.…”

“…GO and KEGG enrichment of differentially expressed genes associated with pheomelanin pigmentation in chickens has been reported by Zheng et al . (2020). These authors indicated that metabolic pathways, melanogenesis, cytoplasm and cell–cell signaling are involved in plumage coloration, which is in agreement with the present study.…”

“…The study of epistasis can be interesting because epistatic interactions aid understanding of the functional relations of genes involved in the trait under study and sometimes can compensate for a lack of additive genome-wide studies in quantitative traits (Visscher et al 2012(Visscher et al , 2017Lee et al 2016). Distinct genes in chickens control plumage color traits (Li et al 2019a,b) and the genes associated with plumage pigmentation, such as melanocortin 1 receptor (MC1R; Kerje et al 2003;Hoque et al 2013;Zhang et al 2013;Ran et al 2016;Tu et al 2019;Yang et al 2019), tyrosinase (TYR;Yang et al 2019;Zheng et al 2020), premelanosome protein (PMEL; Kerje et al 2004;Abolins-Abols et al 2018;Zheng et al 2020), melanophilin (MLPH;Vaez et al 2008;Bed'hom et al 2012), Agouti signaling protein (ASIP; Robic et al 2019;Yang et al 2019), SRY-box (SOX families; Harris et al 2010;Gunnarsson et al 2011), solute carrier family member 2 (SLC45A2; Gunnarsson et al 2007;Zheng et al 2020) and endothelin B2 receptor (EDNRB2; Kinoshita et al 2014;Li et al 2015;Wu et al 2017;Xi et al 2020), are well known. Accordingly, multiple responsible genes have been reported for plumage color variation, but studies have focused on single loci with a major effect, rather than effective modifier loci with small or epistatic effects that influence plumage color more delicately.…”

Origin, Phenotypes, and Plumage Coloration of Golden Pelung Chicken Progenies (G. gallus, Linn.1758)

“…The future is here as it has been proven by numerous pioneering studies in the chicken selective breeding programme around the world with a various approach such as phenomics, sequencing analysis [78,35], transcriptome analysis [57,94], QTL mapping of complex traits [14,30,20], and genome-wide association study [62,2,30,50]. This study demonstrated the possibility of using a genetic marker in the selective breeding programme of golden Pelung chicken with the addition of conventional approaches like morphometrical analysis and phenotypes observation.…”

“…The plumage pigmentation depends on several pigments, including carotenoid, melanin (eumelanin and pheomelanin), porphyrins, avins, psittacofulvins, pterins, purines, and turacin[26, 16,24, 76,20,94]. The two most common and widely found among birds, in particular chickens, are melanin and carotenoid.…”