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Review: cornification, morphogenesis and evolution of feathers

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Abstract

Feathers are corneous microramifications of variable complexity derived from the morphogenesis of barb ridges. Histological and ultrastructural analyses on developing and regenerating feathers clarify the three-dimensional organization of cells in barb ridges. Feather cells derive from folds of the embryonic epithelium of feather germs from which barb/barbule cells and supportive cells organize in a branching structure. The following degeneration of supportive cells allows the separation of barbule cells which are made of corneous beta-proteins and of lower amounts of intermediate filament (IF)(alpha) keratins, histidine-rich proteins, and corneous proteins of the epidermal differentiation complex. The specific protein association gives rise to a corneous material with specific biomechanic properties in barbules, rami, rachis, or calamus. During the evolution of different feather types, a large expansion of the genome coding for corneous feather beta-proteins occurred and formed 3–4-nm-thick filaments through a different mechanism from that of 8–10 nm IF keratins. In the chick, over 130 genes mainly localized in chromosomes 27 and 25 encode feather corneous beta-proteins of 10–12 kDa containing 97–105 amino acids. About 35 genes localized in chromosome 25 code for scale proteins (14–16 kDa made of 122–146 amino acids), claws and beak proteins (14–17 kDa proteins of 134–164 amino acids). Feather morphogenesis is periodically re-activated to produce replacement feathers, and multiple feather types can result from the interactions of epidermal and dermal tissues. The review shows schematic models explaining the translation of the morphogenesis of barb ridges present in the follicle into the three-dimensional shape of the main types of branched or un-branched feathers such as plumulaceous, pennaceous, filoplumes, and bristles. The temporal pattern of formation of barb ridges in different feather types and the molecular control from the dermal papilla through signaling molecules are poorly known. The evolution and diversification of the process of morphogenesis of barb ridges and patterns of their formation within feathers follicle allowed the origin and diversification of numerous types of feathers, including the asymmetric planar feathers for flight.

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Acknowledgments

The study was self-supported (Comparative Histolab) and through local Grants from the University of Bologna during 2004–2010. Dr. Luisa Dalla Valle (University of Padova, Italy) probed the chick genome and Dr. Mattia Toni (University of Bologna, Italy) helped with the assemblage of these protein sequences (Figs. 1S and 2S), and elaborated graphically my manual drawings using the Corel-draw Program. An anonymous referee improved the presentation of the MS.

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  1. Comparative Histolab and Department of BIGEA, University of Bologna, via Selmi 3, 40126, Bologna, Italy

    Lorenzo Alibardi

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  1. Lorenzo Alibardi
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Correspondence to Lorenzo Alibardi.

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Fig. 1S

Stereomicroscopic view of developing downfeathers embedded in resin before sectioning (a–e), mature (f), and a pennaceous feather (g) of the zebra finch. a Feather filament through the transparent sheath (arrowheads) the long barb ridges (arrows) and barbules (double arrowhead). Bar 0.1 mm. b Base of the feather filament to show barbules (arrow) and the forming basal calamus (arrowhead). Bar 0.1 mm. c Close-up of barbules (arrowheads) inserting into barbs. Bar 0.1 mm. d Maturing downfeather showing separated barbs (arrows) and barbules (arrowheads). Bar 0.1 mm. e Other details on separated barbs (arrows) and barbules (arrowheads) formed in the lowermost part of maturing downfeather. Bar 0,1 mm. f Downfeather with separated barbs after the sheath has been shed. Bar 0.5 mm. g Pennaceous feather still emerging from the sheath (arrowhead) but showing the planar vane formed by extending barbs (arrows) from the central rachis (double arrow). Bar 0.2 mm (JPG 2172 kb)

Fig. 2S

Colored amino acid sequences of the 35 KAbetaPs (or CbetaPs), formerly termed beta-keratins), found in chromosome 25 (CR) of the chick, derived from probing the genome with known nucleotide sequences from chick and reptilian beta-proteins at http://genome.ucsc.edu. Although the expression sites for most of these proteins are not known, the glycine-rich region and relative high number of amino acids indicates that these proteins are present in scales, claws and beaks, and few are present in feathers. The accession numbers in the chick genome database are reported on the side (Gallus-Keratin-chromosome n.). Four key amino acids (glycine in red, proline in blue, cysteine in green, and serine in yellow) are indicated to compare their localization in similar proteins of feathers seen in Fig. 2S. The core-box of 20 amino acids is boxed and contains proline-rich regions with high homology with reptilian beta-proteins and includes the beta-folded regions utilized for the polymerization of these proteins (see secondary prediction in Fig. 2b). (JPG 5174 kb)

Fig. 3S

Colored amino acid sequences of the identified 67 feather beta-proteins mostly found in chromosome 27 of the chick (indicates an uncertain, long sequence) and other indicated chromosomes (CR). These shorter sequences in comparison to most of the sequences shown in the previous figure derived from probing the genome with known nucleotide sequences from the chick and reptilian beta-proteins at http://genome.ucsc.edu) and resemble previously known feather keratins (Gregg et al. 1983, 1984). It is unknown which of these proteins are present in different feathers (down, filoplumes, bristles, symmetric or asymmetric feathers) since expression studies form most of these proteins are not available. Other homologous feather proteins present in chromosome 25 (21 sequences) and in few other chromosomes (indicated by arrows or numbers) are shown. Some sequences may represent proteins that are expressed in scale or beak aside feathers. All these proteins present the core-box region (boxed), indicating that they originated from a common, reptilian progenitor protein (JPG 4105 kb)

Fig. 4S

Histology of downfeathers in chick (a–i) and zebra finch (j–m), showing their progressive cornification. a Feather filament at stage 37 showing barb ridges in longitudinal section (arrows). Arrowheads indicate the covering sheath. Bar 100 μm. b Cross-sectioned tip of feather filament at stage 37 showing the circular epithelium (e, outlined by dashes) covered by the stratified sheath (arrowhead) and the central mesenchyme (m). Bar 10 μm. c Detail of forming barb ridge at the mid-level of a feather filament at stage 37 (dashes indicate the borders; the arrowhead points to the sheath) in contact with the mesenchyme (m). Bar 10 μm. d Cross-section near the tip of a feather filament at stage 38 surrounded by a cornified sheath (arrowhead) and containing barbs composed only of the ramus (arrow). Bar 10 μm. e Other apical part of mature feather filaments at stage 39 showing centered barbs with no barbules that are detaching from the cornified sheath (arrowhead) by the degeneration of barb vane cells (v). Bar 10 μm. f Detail of a maturing barb ridge at stage 38 at mid-level of a feather filament showing the two barbule plates (arrowheads) separated by the pale axial plate occupied by barb vane ridge cells (v), and in contact with the sheath (sh). The ramus area shows the vacuolated barb medullary cells (bm) surrounded by barb cortical cells (arrows) Bar 10 μm. g Cross-sectioned mid-level of a natal downfeather at stage 38, showing cornified barbule plates (arrows) surrounded by a corneous sheath (arrowhead). Barb ridges are “embedded” in the epithelium of marginal plates (e). Most blood vessels (ve) at this stage appear empty, probably degenerating. Bar 20 μm. h Longitudinal section showing barb ridges separated by the marginal cell epithelium (e). Piled barb medullary cells (bm) are surrounded by barb cortical cells (arrows). Bar 10 μm. i Detail of the separation of adjacent chains (arrowheads) of barbule cells (bl) from barb cortical (bc) and barb medullary cells (bm) by barb vane ridge cells (v). Bar 10 μm. j Detail showing barb vane cells (v) penetrating between barbule chains (bl), and in continuity with the epithelium (e) of marginal plates. Bar 10 μm. k Detail of a longitudinal section of a feather filament at stage 38 showing maturing barbules (bl) attached to the ramus (bc barb cortical cells; bm barb medullary cells), that alternate with the pale barb vane ridge cells columns (v). Bar 10 μm. l The branched barbules in this longitudinal section at a slightly upper level with respect to the previous figure, are here separated by empty spaces previously occupied by barb vane ridge cells (v). Also, barb cortical cells (bc) are cornified while barb medullary cells are degenerating. The arrowhead indicates the sheath. Bar 10 μm. m Mature barb at about 16 days in ovo featuring the central ramus (ra) and the lateral barbules (bl). Bar 10 μm (JPG 3361 kb)

Fig. 5S

Immunofluorescence (a-e, bars in all figures = 10 μm) and immunogold ultrastructural localization (f–h) using a “feather keratin” antibody (Sawyer et al. 2000; details in Alibardi et al. 2006). a Alligator embryonic epidermis at stage 24 (Hamburger-Hamilton) of a trunk scale with intensely labeled subperiderm layer (arrow). b Chick scutate scale at stage 38 with labeled subperiderm layer (arrow). c Labeled barb ridges in a cross-sectioned developing chick wing feather at stage 38. d Mid-section of a calamus of a zebra finch wing feather seen in cross-section. e Immunolabeled barbules (bl), barb cortical (c) and medullary cells (m) in a longitudinally sectioned chick wing downfeather at stage 38 (d, dermal core). f Immunolabeled corneous material (arrowhead) associated to dense coarse filaments (arrows) in subperiderm cell of the embryonic epidermis of alligator at stage 24. Bar 300 nm. g Immunolabeling in the pale corneous material of subperiderm cells (sp) in chick embryonic scale epidermis at stage 38. The unlabeled outer (p1) and inner (p2) periderm layers contain periderm granules (arrowheads). Bar 300 nm. h Immunolabeled corneous filaments are accumulating in barbule cells of chick wing downfeather at stage 38. Bar 250 nm (JPG 421 kb)

Fig. 6S

Histological cross-sections (a, b, d–g) and longitudinal section (c) of pennaceous feathers (a–e) and bristles (f, g). a Basal part of a follicle in zebrafinch showing the gradual formation of barb ridges from the ventral locus (arrow). The arrowhead indicates the sheath. Bar 20 μm. b Cross-sectioned apical part of juvenile feather follicle in zebra finch, featuring the numerous barb ridges filling the inner surface of the follicle from the ventral locus (arrow) to the opposite rachidial ridge (arrowhead). Bar 20 μm. c Detail of branched barb with barbules, barb cortical and medullary cells in regenerating chick contour feather. Bar 10 μm. d top part of the follicle of a chicken asymmetric feather showing more numerous barb ridges on the left with respect to the right side reaching the ventral locus (arrow). The latter is not centered with the rachis (arrowhead). Bar 100 μm. e Detail on a forming rachidial ridge with the more external cells (asterisk) in course of cornification. Bar 20 μm. f Follicle of ostrich neck bristles showing that few barb ridges are formed while a large part of the collar (included between the double arrow) is occupied by the rachidial ridge. Bar 20 μm. g Follicle of a maturing ostrich bristle showing few barbs (arrows) and a large rachis. Bar 50 μm. bc barb cortical cells, bl barbules, bm barb medullary cells, br barb ridges, e epithelium of marginal plates, p pulp (loose connective), rac rachis/rachidial ridge, sh sheath (JPG 5186 kb)

Fig. 7S

Microscopic detail of barb ridges in a regenerating feather (a), with a schematic drawing of a regenerated feather (b) and its parts (c–f). a Some fibroblasts (arrows) insinuate between barb ridges (br) surrounded externally by the sheath (sh). Bar 20 μm. b Inside the follicle, an enlargement of the dermal papilla (c) shows the different regions. The arrows indicate a low section of the collar (d), a higher section of the collar at the beginning (e) or more advanced (f) formation of barb ridges formation. The circle (f) is enlarged (g) to show the cell interaction of the fibroblasts of the dermal papilla with the forming barb ridges (JPG 648 kb)

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Alibardi, L. Review: cornification, morphogenesis and evolution of feathers. Protoplasma 254, 1259–1281 (2017). https://doi.org/10.1007/s00709-016-1019-2

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