Genomic organization and molecular phylogenies of the beta (β) keratin multigene family in the chicken (Gallus gallus) and zebra finch (Taeniopygia guttata): implications for feather evolution

Department of Biological Sciences, University of South Carolina, Columbia, SC 29205, USA.
BMC Evolutionary Biology (Impact Factor: 3.37). 05/2010; 10(1):148. DOI: 10.1186/1471-2148-10-148
Source: PubMed

ABSTRACT The epidermal appendages of reptiles and birds are constructed of beta (beta) keratins. The molecular phylogeny of these keratins is important to understanding the evolutionary origin of these appendages, especially feathers. Knowing that the crocodilian beta-keratin genes are closely related to those of birds, the published genomes of the chicken and zebra finch provide an opportunity not only to compare the genomic organization of their beta-keratins, but to study their molecular evolution in archosaurians.
The subfamilies (claw, feather, feather-like, and scale) of beta-keratin genes are clustered in the same 5' to 3' order on microchromosome 25 in chicken and zebra finch, although the number of claw and feather genes differs between the species. Molecular phylogenies show that the monophyletic scale genes are the basal group within birds and that the monophyletic avian claw genes form the basal group to all feather and feather-like genes. Both species have a number of feather clades on microchromosome 27 that form monophyletic groups. An additional monophyletic cluster of feather genes exist on macrochromosome 2 for each species. Expression sequence tag analysis for the chicken demonstrates that all feather beta-keratin clades are expressed.
Similarity in the overall genomic organization of beta-keratins in Galliformes and Passeriformes suggests similar organization in all Neognathae birds, and perhaps in the ancestral lineages leading to modern birds, such as the paravian Anchiornis huxleyi. Phylogenetic analyses demonstrate that evolution of archosaurian epidermal appendages in the lineage leading to birds was accompanied by duplication and divergence of an ancestral beta-keratin gene cluster. As morphological diversification of epidermal appendages occurred and the beta-keratin multigene family expanded, novel beta-keratin genes were selected for novel functions within appendages such as feathers.

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Available from: Roger H. Sawyer, Sep 27, 2015
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    • "The expansion of a-keratin genes may have contributed to the independent origin of hair and nails in mammals and baleen in whales (Vandebergh and Bossuyt, 2012). Largescale expansions of b-keratin genes in birds and turtles may be involved in the innovation of the feathers and turtle shells (Greenwold and Sawyer, 2010; Li et al., 2013b). In a recent study, we carried out an exhaustive search of a-and b-keratin genes in the Galgal4 genome assembly and characterized the expression pattern of some keratin genes. "
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    ABSTRACT: How tissue patterns form in development and regeneration is a fundamental issue remaining to be fully understood. The integument often forms repetitive units in space (periodic patterning) and time (cyclic renewal), such as feathers and hairs. Integument patterns are visible and experimentally manipulatable, helping us reveal pattern formative processes. Variability is seen in regional phenotypic specificities and temporal cycling at different physiological stages. Here we show some cellular/molecular bases revealed by analyzing integument patterns. 1) Localized cellular activity (proliferation, rearrangement, apoptosis, differentiation) transforms prototypic organ primordia into specific shapes. Combinatorial positioning of different localized activity zones generates diverse and complex organ forms. 2) Competitive equilibrium between activators and inhibitors regulates stem cells through cyclic quiescence and activation. Dynamic interactions between stem cells and their adjacent niche regulate regenerative behavior, modulated by multi-layers of macro-environmental factors (dermis, body hormone status and external environment). Genomics studies may reveal how positional information of localized cellular activity is stored. In vivo skin imaging and lineage tracing unveils new insights into stem cell plasticity. Principles of self-assembly obtained from the integumentary organ model can be applied to help restore damaged patterns during regenerative wound healing and for tissue engineering to rebuild tissues. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    Developmental Dynamics 04/2015; 244(8). DOI:10.1002/dvdy.24281 · 2.38 Impact Factor
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    • "Clade C6 consists of the feather , feather‐like and BKJ genes from the chicken and zebra finch ( Fig . 2 ) . The feather‐like b‐keratins on microchromosome 25 of the chicken and zebra finch and the BKJ genes ( similar to feather‐like genes on chromosome 6 of the chicken ) are the basal genes , giving rise to the feather b‐keratins on microchromosome 25 , chromosome 2 , and microchromosome 27 of the chicken and zebra finch ( Greenwold and Sawyer , 2010 ) ( Fig . S1 ) . "
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    ABSTRACT: The archosauria consist of two living groups, crocodilians, and birds. Here we compare the structure, expression, and phylogeny of the beta (β)-keratins in two crocodilian genomes and two avian genomes to gain a better understanding of the evolutionary origin of the feather β-keratins. Unlike squamates such as the green anole with 40 β-keratins in its genome, the chicken and zebra finch genomes have over 100 β-keratin genes in their genomes, while the American alligator has 20 β-keratin genes, and the saltwater crocodile has 21 β-keratin genes. The crocodilian β-keratins are similar to those of birds and these structural proteins have a central filament domain and N- and C-termini, which contribute to the matrix material between the twisted β-sheets, which form the 2-3 nm filament. Overall the expression of alligator β-keratin genes in the integument increases during development. Phylogenetic analysis demonstrates that a crocodilian β-keratin clade forms a monophyletic group with the avian scale and feather β-keratins, suggesting that avian scale and feather β-keratins along with a subset of crocodilian β-keratins evolved from a common ancestral gene/s. Overall, our analyses support the view that the epidermal appendages of basal archosaurs used a diverse array of β-keratins, which evolved into crocodilian and avian specific clades. In birds, the scale and feather subfamilies appear to have evolved independently in the avian lineage from a subset of archosaurian claw β-keratins. The expansion of the avian specific feather β-keratin genes accompanied the diversification of birds and the evolution of feathers. J. Exp. Zool. (Mol. Dev. Evol.) 9999B: XX-XX, 2013. © 2013 Wiley Periodicals, Inc.
    Journal of Experimental Zoology Part B Molecular and Developmental Evolution 09/2013; 320(6). DOI:10.1002/jez.b.22514 · 2.31 Impact Factor
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    • "Phylogenetic analysis demonstrated that evolution of archosaurian epidermal appendages in the linage leading to birds was accompanied by duplication and divergence of the ancestral ß-keratin gene cluster. In the chicken, four subfamilies (claw, feather, feather-like and scale) of the ß-keratin genes have been named in accordance with tissue-specific expression and sequence heterogeneity [27]. These ß-keratin gene subfamilies are clustered on GGA25 whereas the genes for two other monophyletic groups of feather keratins are located on GGA27 and GGA2 respectively. "
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    ABSTRACT: Background Detecting genetic variation is a critical step in elucidating the molecular mechanisms underlying phenotypic diversity. Until recently, such detection has mostly focused on single nucleotide polymorphisms (SNPs) because of the ease in screening complete genomes. Another type of variant, copy number variation (CNV), is emerging as a significant contributor to phenotypic variation in many species. Here we describe a genome-wide CNV study using array comparative genomic hybridization (aCGH) in a wide variety of chicken breeds. Results We identified 3,154 CNVs, grouped into 1,556 CNV regions (CNVRs). Thirty percent of the CNVs were detected in at least 2 individuals. The average size of the CNVs detected was 46.3 kb with the largest CNV, located on GGAZ, being 4.3 Mb. Approximately 75% of the CNVs are copy number losses relatively to the Red Jungle Fowl reference genome. The genome coverage of CNVRs in this study is 60 Mb, which represents almost 5.4% of the chicken genome. In particular large gene families such as the keratin gene family and the MHC show extensive CNV. Conclusions A relative large group of the CNVs are line-specific, several of which were previously shown to be related to the causative mutation for a number of phenotypic variants. The chance that inter-specific CNVs fall into CNVRs detected in chicken is related to the evolutionary distance between the species. Our results provide a valuable resource for the study of genetic and phenotypic variation in this phenotypically diverse species.
    BMC Genomics 06/2013; 14(1):398. DOI:10.1186/1471-2164-14-398 · 3.99 Impact Factor
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