The morphogenesis of feathers - PubMed (original) (raw)

. 2002 Nov 21;420(6913):308-12.

doi: 10.1038/nature01196. Epub 2002 Oct 30.

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The morphogenesis of feathers

Mingke Yu et al. Nature. 2002.

Abstract

Feathers are highly ordered, hierarchical branched structures that confer birds with the ability of flight. Discoveries of fossilized dinosaurs in China bearing 'feather-like' structures have prompted interest in the origin and evolution of feathers. However, there is uncertainty about whether the irregularly branched integumentary fibres on dinosaurs such as Sinornithosaurus are truly feathers, and whether an integumentary appendage with a major central shaft and notched edges is a non-avian feather or a proto-feather. Here, we use a developmental approach to analyse molecular mechanisms in feather-branching morphogenesis. We have used the replication-competent avian sarcoma retrovirus to deliver exogenous genes to regenerating flight feather follicles of chickens. We show that the antagonistic balance between noggin and bone morphogenetic protein 4 (BMP4) has 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 inducing apoptosis of the marginal plate epithelia, which results in spaces between barbs. Our analyses identify the molecular pathways underlying the topological transformation of feathers from cylindrical epithelia to the hierarchical branched structures, and provide insights on the possible developmental mechanisms in the evolution of feather forms.

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Conflict of interest statement

Competing interests statement

The authors declare that they have no competing financial interests.

Figures

Figure 1

Figure 1

Feather branching morphogenesis and gene expression. a, Diagram showing the three branching levels. Level I: Rachis (blue) branches into barbs (red). Ia, radially and Ib, bilaterally symmetric feathers. Level II: Barbs branch into barbules (green); Level III: Barbules branch into cilia and hooklets (purple). b, Different chicken feather types. c, Feather follicle structure schematic. d–f, BMP4, Noggin, and BMP2 expression patterns. The two dotted lines indicate the level of cross sections shown in Supplementary Information Fig. 2. g, Schematic drawing of feather barb. h, I, BMP2 in barb ridges. First in peripheral marginal plates (mp), then switch to barbule plates (bp). dp, dermal papilla; rz, ramogenic zone. Bar size, 100 μm.

Figure 2

Figure 2. Phenotypic changes in feathers regenerated from follicles injected with RCAS-Noggin, BMP4, and BMP2 respectively

a, Diagram showing the gene expression strategy. b, X-gal staining of a regenerating feather follicle injected with RCAS-LacZ 7 days ago. c–f, Splitting or merging of the rachis is indicated by red arrows. g–j, Alteration of the barbs. Abnormal branch points are indicated by blue arrows. k, Diagram illustrating the overall phenotypic changes. Bar size, 50 μm (c–f, l, j), 100 μm (g, h).

Figure 3

Figure 3. Analyses of feathers injected with RCAS-Noggin, -BMP4, and -BMP2 respectively

a–d, Cross sections. e–l, Changes in barb ridges. m–p, Changes of rachidial ridge size (H&E). Rachis width (green arc). p, Enlarged indicated area (see inset) is part of the rachidial structure, not barb ridges (compare with Fig. 3e). q–t, ISH with SHH probes. Marginal plates or comparable regions (red arrows). u–x, ISH with feather keratin probes. Green lines delineate barb ridges. Dotted lines indicate abnormal barb ridges. rr, rachidial ridge. mp, marginal plate. bp, barbule plate. ap, axial plate. gz, barb ridge growth zone. Bar size, 100μm.

Figure 4

Figure 4. SHH roles in barb formation

a, Normal feather whole mount ISH of SHH and BMP2. b, SHH inhibition by RCAS-antisense Shh or cyclopamine produced fused vanes. c, Schematic depicting changes in b. Barbs (red). Barbules (green). d, Cross sections (H&E) showed barb ridge segments that failed to separate varying from more severe (5–9 o’clock region) to less severe (1–2 o’clock). e, Enlarged indicated area in d. f, g, Apoptosis in late-differentiated barb ridges in normal and SHH suppressed follicles. bp, barbule plate; mp, marginal plate; fs, feather sheath; pe, pulp epithelium. Bar size, 100μm.

Figure 5

Figure 5. Models of feather branching and evolution of feather forms

a, Roles of Noggin/BMP4, Shh, BMP2 in the 3 levels of feather branching. b, The ratio of noggin and BMP4 may determine the number and size of barb ridges. A localized high BMP/noggin ratio, together with a helical growth mode of barb ridges, can lead to the formation of a rachidial ridge through fusion of barb ridges. c, Hypothetical models of the evolution of feather forms. Upper row, Barb → Rachis model. Lower row, Rachis→Barb model. The experimental data are in favor of the Barb → Rachis model.

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