Topographical mapping of α- and β-keratins on developing chicken skin integuments: Functional interaction and evolutionary perspectives

Abstract

Avian integumentary organs include feathers, scales, claws, and beaks. They cover the body surface and play various functions to help adapt birds to diverse environments. These keratinized structures are mainly composed of corneous materials made of α-keratins, which exist in all vertebrates, and β-keratins, which only exist in birds and reptiles. Here, members of the keratin gene families were used to study how gene family evolution contributes to novelty and adaptation, focusing on tissue morphogenesis. Using chicken as a model, we applied RNA-seq and in situ hybridization to map α-and β-keratin genes in various skin appendages at embryonic developmental stages. The data demonstrate that temporal and spatial α-and β-keratin expression is involved in establishing the diversity of skin appendage phenotypes. Embryonic feathers express a higher proportion of β-keratin genes than other skin regions. In feather filament morphogenesis, β-keratins show intricate complexity in diverse substructures of feather branches. To explore functional interactions, we used a retrovirus transgenic system to ectopically express mutant α-or antisense β-keratin forms. α-and β-keratins show mutual dependence and mutations in either keratin type results in disrupted keratin networks and failure to form proper feather branches. Our data suggest that combinations of α-and β-keratin genes contribute to the morphological and structural diversity of different avian skin appendages, with feather-β-keratins conferring more possible composites in building intrafeather architecture complexity, setting up a platform of morphological evolution of functional forms in feathers.skin appendage | feather | scale | claw | beak | Evo-Devo

Sauropsids Cornification is Based on Corneous Beta‐Proteins, a Special Type of Keratin‐Associated Corneous Proteins of the Epidermis

“…">Sauropsid CβPs determine the cornification of the cells where they are accumulated, not their keratinization, and therefore sauropsid scales, claws, beaks, and feathers are corneous structures and not keratinized structures. Feathers in particular contain keratins of IF‐type and of β‐type, which should not be termed feather keratins (Greenwold and Sawyer, , , ; Greenwold et al., ; Ng et al., ; Wu et al., ). Also for this reason, one should not use “feather/beta‐keratins” for a cornification process where other proteins are also involved.…”

“…These filamentous proteins were adaptive for sauropsids and their genes within the EDC duplicated considerably. Later, with the diversification of the C‐ and N‐terminals in different groups of sauropsids, these proteins were utilized for specialized skin appendages, initially scales and claws, and later beaks, pad lamellae (adhesive scale modifications in lizards), and feathers in some dinosaurs and birds (Li et al., ; Greenwold et al., ; Ng et al., ; Wu et al., ). The evolution of feathers likely took place expanding the genes encoding small CFβPs in conjunction with the origin of the morphogenetic process of barb ridge formation in archosaurians (Alibardi et al., ; Alibardi, ; Greenwold and Sawyer, , , ).…”

Microscopic and immunohistochemical analyses of the claw of the nesting dinosaur, Citipati osmolskae

“…Beta-keratins (or 'corneous beta-proteins' [7][8][9][10]) are insoluble, rigid, fibrous, structural proteins distinct from alpha-keratins in composition and structure. They are expressed only in reptiles and birds (sauropsids) [11][12][13], suggesting that this gene family originated after the divergence of sauropsids from other vertebrates [5,[14][15][16]. The beta-keratins have in common a core of approximately 30 amino acids and produce filaments (microfibrils) 3 nm in diameter [17].…”

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

“…Even though most chicken CBP subfamilies are expressed during embryonic development of scales and feathers, they are differentially expressed within the EDC locus (microchromosome 25; Greenwold et al, ). Furthermore differential feather CBPs expression has been reported for various feather loci (Greenwold et al, ; Ng et al, ), and in different feather types and various parts of feathers (Alibardi, ; Greenwold et al, ; Ng et al, ; Wu et al, ). The finding of differential CBP and IF‐keratin expression in feathers was mapped to all embryonic chicken appendages (indicated as beta‐keratins and alpha‐keratins in Wu et al, ).…”