The morphogenesis of feathers

Abstract

The most unique character of the feather is its highly ordered hierarchical branched structure 1, 2 . This evolutionary novelty confers flight function to birds [3][4][5] . Recent discoveries of fossils in China have prompted keen interest in the origin and evolution of feathers [6][7][8][9][10][11][12][13][14] . However, controversy arises whether the irregularly branched integumentary fibers on dinosaurs such as Sinornithosaurus are truly feathers 6,11 , and whether an integumentary appendage with a major central shaft and notched edges is a non-avian feather or a proto-feather [8][9][10] . Here we take a developmental approach to analyze molecular mechanisms in feather branching morphogenesis. We have used the replication competent avian sarcoma (RCAS) retrovirus 15 to efficiently deliver exogenous genes to regenerating chicken flight feather follicles. We show that the antagonistic balance between noggin and bone morphogenetic protein 4 (BMP4) plays a critical role in feather branching, with BMP4 promoting rachis formation and barb fusion, and noggin enhancing rachis and barb branching. Furthermore we show that sonic hedgehog (SHH) is essential for apoptosis of the marginal plate epithelia to become spaces between barbs. Our analyses show the molecular pathways underlying the topological transformation of feathers from cylindrical epithelia to the hierarchical branched structures, and provide first clues on the possible developmental mechanisms in the evolution of feather forms.With three branching levels, i.e. from rachis to barbs; from barbs to barbules and from barbules to cilia or hooklets 1 (Fig. 1a), feathers can develop into a variety of forms, including the downy, contour, flight feathers, etc. (Fig. 1b). As in hairs, the feather follicle is composed of a dermal papilla and epidermal collar (equivalent to the hair matrix, Fig. 1c-f). Through epithelial-mesenchymal interactions, the epithelial cells at the bottom of the follicle undergo active proliferation (proliferation zone, Fig. 1c). Immediately above, the epithelial cells start to form the rachidial ridge and the barb ridges (ramogenic zone, Fig. 1c, f) [16][17][18][19] . Further distal, the barb ridge epithelia actively proliferate and differentiate to form the marginal plates, barbule plates and axial plates (Fig. 1e, central part). The barb ridges grow to form barbs, composed of the ramus and barbules, while the marginal and axial plate cells die to become the intervening space. Individual barbule plate cells undergo further cell shape changes to form the cilia and hooklets 1 . The barb ridges fused proximally to form the Correspondence and requests for materials should be addressed to: Cheng-Ming Chuong, chuong@pathfinder.usc.edu. Competing interests statementThe authors declare that they have no competing financial interests. Fig. 1) illustrate this process. HHS Public AccessThe cellular and molecular mechanisms of epithelial organ morphogenesis are beginning to be understood 20,21 . While branching morphogenesis 21 has been studied...

Adaptation to the sky: Defining the feather with integument fossils from mesozoic China and experimental evidence from molecular laboratories

“…These data suggest that the BMP pathway is involved in feather branching ( Fig. 3E; Yu et al, 2002).…”

“…In view of its existence only on the tail, it appears that these are specialized feathers and the giant shaft is more likely to be secondarily derived for specialized functions as discussed above. Recent molecular data (Yu et al, 2002) also offers an explanation through a developmental mechanism that such a giant shaft can be produced by over-production of BMP.…”

“…Noggin, a BMP antagonist, was expressed as a gradient in the pulp, with the highest expression levels found at the ramogenic zone. To further explore the role of this pathway in branching morphogenesis, we used the RCAS retrovirus to deliver noggin to regenerating feather follicles of modern chickens (Yu et al, 2002). The resulting rachidial ridges were severely fragmented.…”

“…However, it has been difficult to do molecular analyses of later events in feather morphogenesis. The novel plucking / regeneration / molecular mis-expression feather model developed by Yu et al, (2002;and Fig. 3C, D) has opened a new way to analyze the forms of adult feathers.…”

Morphoregulation of avian beaks: Comparative mapping of growth zone activities and morphological evolution

“…In situ hybridization and immunohistochemistry were performed as described (Jiang et al, 1998), and some were performed using the automated Ventana Discovery system. X-gal staining was performed according to Yu et al (2002). Cartilage and bone were stained as described by MonsoroBurq et al (1994) using Alcian blue and Alizarin red, respectively.…”