Immunolocalization of a Histidine-Rich Epidermal Differentiation Protein in the Chicken Supports the Hypothesis of an Evolutionary Developmental Link between the Embryonic Subperiderm and Feather Barbs and Barbules

Alibardi, Lorenzo; Holthaus, Karin Brigit; Sukseree, Supawadee; Hermann, Marcela; Tschachler, Erwin; Eckhart, Leopold

doi:10.1371/journal.pone.0167789

Cited by 23 publications

(40 citation statements)

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“…This hypothesis is supported by the expression of β-keratins, EDCRP (epidermal differentiation cysteine-rich protein) and EDMTFH (epidermal differentiation protein starting with an MTF motif and rich in histidine) both in the barb and barbule cells of developing feathers and in the subperiderm layer of the embryonic epidermis, implying a topological and developmental relationship between embryonic subperiderm and feather barbs and barbules ( Strasser et al. 2015 ; Alibardi et al. 2016 ).…”

Section: Diversity Of Feather Morphotypementioning

confidence: 93%

Genetic and Molecular Basis of Feather Diversity in Birds

2018

Genome Biology and Evolution

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Feather diversity is striking in many aspects. Although the development of feather has been studied for decades, genetic and genomic studies of feather diversity have begun only recently. Many questions remain to be answered by multidisciplinary approaches. In this review, we discuss three levels of feather diversity: Feather morphotypes, intraspecific variations, and interspecific variations. We summarize recent studies of feather evolution in terms of genetics, genomics, and developmental biology and provide perspectives for future research. Specifically, this review includes the following topics: 1) Diversity of feather morphotype; 2) feather diversity among different breeds of domesticated birds, including variations in pigmentation pattern, in feather length or regional identity, in feather orientation, in feather distribution, and in feather structure; and 3) diversity of feathers among avian species, including plumage color and morph differences between species and the regulatory differences in downy feather development between altricial and precocial birds. Finally, we discussed future research directions.

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Section: Diversity Of Feather Morphotypementioning

confidence: 93%

Genetic and Molecular Basis of Feather Diversity in Birds

2018

Genome Biology and Evolution

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“…2015 ), Epidermal Differentiation Cysteine-Rich Protein ( EDCRP ) in feathers ( Strasser et al. 2015 ) and Epidermal Differentiation Protein starting with a MTF motif and rich in Histidine ( EDMTFH ) in feathers ( Alibardi et al. 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Comparative Analysis of Epidermal Differentiation Genes of Crocodilians Suggests New Models for the Evolutionary Origin of Avian Feather Proteins

Holthaus

Strasser

Lachner

et al. 2018

Genome Biology and Evolution

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The epidermis of amniotes forms a protective barrier against the environment and the differentiation program of keratinocytes, the main cell type in the epidermis, has undergone specific alterations in the course of adaptation of amniotes to a broad variety of environments and lifestyles. The epidermal differentiation complex (EDC) is a cluster of genes expressed at late stages of keratinocyte differentiation in both sauropsids and mammals. In the present study, we identified and analyzed the crocodilian equivalent of the EDC. The gene complement of the EDC of both the American alligator and the saltwater crocodile were determined by comparative genomics, de novo gene prediction and identification of EDC transcripts in published transcriptome data. We found that crocodilians have an organization of the EDC similar to that of their closest living relatives, the birds, with which they form the clade Archosauria. Notable differences include the specific expansion of a subfamily of EDC genes in crocodilians and the loss of distinct ancestral EDC genes in birds. Identification and comparative analysis of crocodilian orthologs of avian feather proteins suggest that the latter evolved by cooption and sequence modification of ancestral EDC genes, and that the amplification of an internal highly cysteine-enriched amino acid sequence motif gave rise to the feather component epidermal differentiation cysteine-rich protein in the avian lineage. Thus, sequence diversification of EDC genes contributed to the evolutionary divergence of the crocodilian and avian integuments.

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“…IF‐keratin and CBPs loci are distant and unrelated phylogenetically. CBPs of 8–30 kDa are proteins characterized by a unique amino acid composition and by a central beta‐motif sequence which confers a pleaded beta‐sheet secondary structure to this region of the protein (Fraser & Parry, , ; Calvaresi, Eckhart, & Alibardi, ). CBPs are rich in cysteine whereas numerous IF‐keratins of the epidermis are poor in cysteine and only trichocyte keratins have a higher amount of this amino acid (Eckhart & Ehrlich, ; Steinert & Freedberg, ).…”

Section: Alpha‐keratins (If‐keratins) Versus Beta‐keratins (Cbps)mentioning

confidence: 99%

“…In turtles several CBPs with a quite long N‐terminal rich in proline (30–40%) were found (Holthaus et al , Supporting Information Figure S4). At present the function of these specific proline inserts is unknown, but as they have only been identified in turtles they might be related to the formation of the turtle shell or the rhamphotheca.…”

Section: Conserved and Special Molecular Features Of Cbpsmentioning

confidence: 99%

“…In contrast, other types of EDC genes such as EDAAs positioned in the CBP cluster have largely expanded in crocodilians (Holthaus et al, ) and could have functions similar to CBPs substituting for the CBP expansion seen in other clades. The function of EDAAs, also named EDMTFs in chicken (Strasser et al, ), is not known except for a histidine‐rich member of the chicken (EDMTFH) which has been found in feathers (Alibardi et al, ).…”

Section: Final Evolutionary Considerationsmentioning

confidence: 99%

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Review: Evolution and diversification of corneous beta‐proteins, the characteristic epidermal proteins of reptiles and birds

et al. 2018

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In all amniotes specialized intermediate filament keratins (IF‐keratins), in addition to keratin‐associated and corneous proteins form the outermost cornified layer of the epidermis. Only in reptiles and birds (sauropsids) the epidermis of scales, claws, beaks, and feathers, largely comprises small proteins formerly indicated as “beta‐keratins” but here identified as corneous beta‐proteins (CBPs) to avoid confusion with true keratins. Genes coding for CBPs have evolved within the epidermal differentiation complex (EDC), a locus with no relationship with those of IF‐keratins. CBP genes have the same exon–intron structure as EDC genes encoding other corneous proteins of sauropsids and mammals, but they are unique by encoding a peculiar internal amino acid sequence motif beta‐sheet region that allows formation of CBP filaments in the epidermis and epidermal appendages of reptiles and birds. In contrast, skin appendages of mammals, like hairs, claws, horns and nails, contain keratin‐associated proteins that, like IF‐keratin genes, are encoded by genes in loci different from the EDC. Phylogenetic analysis shows that lepidosaurian (lizards and snakes) and nonlepidosaurian (crocodilians, birds, and turtles) CBPs form two separate clades that likely originated after the divergence of these groups of sauropsids in the Permian Period. Clade‐specific CBPs evolved to make most of the corneous material of feathers in birds and of the shell in turtles. Based on the recent identification of the complete sets of CBPs in all major phylogenetic clades of sauropsids, this review provides a comprehensive overview of the molecular evolution of CBPs.

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Immunolocalization of a Histidine-Rich Epidermal Differentiation Protein in the Chicken Supports the Hypothesis of an Evolutionary Developmental Link between the Embryonic Subperiderm and Feather Barbs and Barbules

Cited by 23 publications

References 50 publications

Genetic and Molecular Basis of Feather Diversity in Birds

Genetic and Molecular Basis of Feather Diversity in Birds

Comparative Analysis of Epidermal Differentiation Genes of Crocodilians Suggests New Models for the Evolutionary Origin of Avian Feather Proteins

Review: Evolution and diversification of corneous beta‐proteins, the characteristic epidermal proteins of reptiles and birds

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