Subdivision of ancestral scale genetic program underlies origin of feathers and avian scutate scales

Musser, Jacob M.; Wagner, Günter P.; Liang, Cong; Stabile, Frank A.; Cloutier, Alison; Baker, Allan J.; Prum, Richard O.

doi:10.1101/377358

Cited by 4 publications

(7 citation statements)

References 53 publications

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“…Consistent with this observation, recent transcriptomic analyses have identified specific ECM genes that are differentially expressed between these epidermal types in developing archosaur embryos , Musser et al, 2018. With the importance of the ECM in mind, we identified ECM genes putatively regulated by PITX1 and/or TBX5 during pigeon limb development by cross-referencing our FL/HL, grouse, and muff gene sets to a list of 491 genes annotated as ECM components in the Gene Ontology database (GO:0031012) (Ashburner et al, 2000, The Gene Ontology, 2017, Carbon et al, 2009.…”

Section: Differentially Expressed Ecm Components In Feathered Hlssupporting

confidence: 52%

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Pigeon foot feathering reveals conserved limb identity networks

Boer

Hollebeke

Park

et al. 2019

Preprint

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statementIn feather-footed pigeons, mutant alleles of PITX1 and TBX5 drive the partial redeployment of an evolutionarily conserved forelimb genetic program in the hindlimb. AbstractThe tetrapod limb is a stunning example of evolutionary diversity, with dramatic variation not only among distantly related species, but also between the serially homologous forelimbs (FLs) and hindlimbs (HLs) within species. Despite this variation, highly conserved genetic and developmental programs underlie limb development and identity in all tetrapods, raising the question of how limb diversification is generated from a conserved toolkit. In some breeds of domestic pigeon, shifts in the expression of two conserved limb identity transcription factors, PITX1 and TBX5, are associated with the formation of feathered HLs with partial FL identity. To determine how modulation of PITX1 and TBX5 expression affects downstream gene expression, we compared the transcriptomes of embryonic limb buds from pigeons with scaled and feathered HLs. We identified a set of differentially expressed genes enriched for genes encoding transcription factors, extracellular matrix proteins, and components of developmental signaling pathways with important roles in limb development. A subset of the genes that distinguish scaled and feathered HLs are also differentially expressed between FL and scaled HL buds in pigeons, pinpointing a set of gene expression changes downstream of PITX1 and TBX5 in the partial transformation from HL to FL identity. We extended our analyses by comparing pigeon limb bud transcriptomes to chicken, anole lizard, and mammalian datasets to identify deeply conserved PITX1-and TBX5-regulated components of the limb identity program. Our analyses reveal a suite of predominantly low-level gene expression changes that are conserved across amniotes to regulate the identity of morphologically distinct limbs.

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Section: Differentially Expressed Ecm Components In Feathered Hlssupporting

confidence: 52%

“…We predict that these unique sets of genes are associated with the development of species-specific limb phenotypes. In support of this idea, specific sets of genes initiate distinct developmental programs to form feathers or different scale types in archosaur embryos (Musser et al, 2018.…”

Section: Embryonic Limb Identity Networkmentioning

confidence: 92%

Pigeon foot feathering reveals conserved limb identity networks

Boer

Hollebeke

Park

et al. 2019

Preprint

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“…Squamates also possess distinct epithelial appendages on the ventral surfaces of their feet. This observation, in combination with the presence of reticulate scales in birds, led to the suggestion that the ancestral archosaur would have also possessed distinct reticulate scales [25]. To test this hypothesis, we examined scale development on the ventral footpad of a reptilian squamate, the bearded dragon ( P. vitticeps ) (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Recent RNA-seq analysis of avian epithelial appendage types has indicated that feathers and scutate scales are more similar to each other, and to alligator scale types, than reticulate scales [25]. Researchers proposed that reticulate scales may have therefore arisen relatively earlier in tetrapod evolution.…”

Section: Discussionmentioning

confidence: 99%

“…Reticulate scales may be distinct from other amniote epithelial appendages due to the apparent lack of individual epithelial placodes [6, 24]. A recent transcriptome sequencing (RNA-seq) analysis showed that gene expression during feather development is more similar to that of scutate scale development than expression during reticulate scale development [25]. One conclusion from this study suggested that reticulate scales are comparatively less derived than feathers and scutate scales, potentially representing a more primitive state.…”

Section: Introductionmentioning

confidence: 94%

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Conserved gene signalling and a derived patterning mechanism underlie the development of avian footpad scales

Cooper

Lloyd

Di‐Poï

et al. 2019

EvoDevo

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Background Vertebrates possess a diverse range of integumentary epithelial appendages, including scales, feathers and hair. These structures share extensive early developmental homology, as they mostly originate from a conserved anatomical placode. In the context of avian epithelial appendages, feathers and scutate scales are known to develop from an anatomical placode. However, our understanding of avian reticulate (footpad) scale development remains unclear. Results Here, we demonstrate that reticulate scales develop from restricted circular domains of thickened epithelium, with localised conserved gene expression in both the epithelium and underlying mesenchyme. These domains constitute either anatomical placodes, or circular initiatory fields (comparable to the avian feather tract). Subsequent patterning of reticulate scales is consistent with reaction–diffusion (RD) simulation, whereby this primary domain subdivides into smaller secondary units, which produce individual scales. In contrast, the footpad scales of a squamate model (the bearded dragon, Pogona vitticeps ) develop synchronously across the ventral footpad surface. Conclusions Widely conserved gene signalling underlies the initial development of avian reticulate scales. However, their subsequent patterning is distinct from the footpad scale patterning of a squamate model, and the feather and scutate scale patterning of birds. Therefore, we suggest reticulate scales are a comparatively derived epithelial appendage, patterned through a modified RD system. Electronic supplementary material The online version of this article (10.1186/s13227-019-0130-9) contains supplementary material, which is available to authorized users.

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Cis -acting mutation affecting GJA5 transcription is underlying the Melanotic within-feather pigmentation pattern in chickens

Lee

Chen

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Melanotic (Ml) is a mutation in chickens that extends black (eumelanin) pigmentation in normally brown or red (pheomelanin) areas, thus affecting multiple within-feather patterns [J. W. Moore, J. R. Smyth Jr, J. Hered. 62, 215–219 (1971)]. In the present study, linkage mapping using a back-cross between Dark Cornish (Ml/Ml) and Partridge Plymouth Rock (ml+/ml+) chickens assigned Ml to an 820-kb region on chromosome 1. Identity-by-descent mapping, via whole-genome sequencing and diagnostic tests using a diverse set of chickens, refined the localization to the genomic region harboring GJA5 encoding gap-junction protein 5 (alias connexin 40) previously associated with pigmentation patterns in zebrafish. An insertion/deletion polymorphism located in the vicinity of the GJA5 promoter region was identified as the candidate causal mutation. Four different GJA5 transcripts were found to be expressed in feather follicles and at least two showed differential expression between genotypes. The results showed that Melanotic constitutes a cis-acting regulatory mutation affecting GJA5 expression. A recent study established the melanocortin-1 receptor (MC1R) locus and the interaction between the MC1R receptor and its antagonist agouti-signaling protein as the primary mechanism underlying variation in within-feather pigmentation patterns in chickens. The present study advances understanding the mechanisms underlying variation in plumage color in birds because it demonstrates that the activity of connexin 40/GJA5 can modulate the periodic pigmentation patterns within individual feathers.

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Subdivision of ancestral scale genetic program underlies origin of feathers and avian scutate scales

Cited by 4 publications

References 53 publications

Pigeon foot feathering reveals conserved limb identity networks

Pigeon foot feathering reveals conserved limb identity networks

Conserved gene signalling and a derived patterning mechanism underlie the development of avian footpad scales

Cis -acting mutation affecting GJA5 transcription is underlying the Melanotic within-feather pigmentation pattern in chickens

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