A Novel Gain-Of-Function Mutation of the Proneural IRX1 and IRX2 Genes Disrupts Axis Elongation in the Araucana Rumpless Chicken

Freese, Nowlan H.; Lam, Brianna A.; Staton, Meg; Scott, Allison; Chapman, Steve

doi:10.1371/journal.pone.0112364

Cited by 24 publications

(33 citation statements)

References 88 publications

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“…The phalloidin and hematoxylin data show that progressively smaller somites form towards the tail tip, and they all form discretely with no evidence of segregation anomalies, including segregation of the most distal somite from posterior mesoderm. This data complements several other studies that show that when somite addition has ceased, undifferentiated mesenchyme remains at the tail tip, distal from the last separate somite, which then undergoes apoptosis 9,23,24 . Our study and those previously reported demonstrate that even the most distal somite segregates, and that all distal somites form discretely.…”

Section: Resultssupporting

confidence: 90%

“…Immunostaining showed that both taper distally, in proportion to the tail profile, and extend to the tail tip. While excess neural differentiation and defects in notochord patterning can cause short and/or fused tails 8,9 , there is no morphological evidence of such events in wildtype chicken development.…”

Section: Development Of Structures In the Pygostyle And Free Vertebramentioning

confidence: 99%

“…A relevant example is the genetic change underlying the truncated tail phenotype in the rumpless araucana chicken. In these birds, tissue that normally contributes to axial extension instead differentiates to a neural fate, resulting in multiple neural tubes, complete loss or reduction of tail vertebrae, and irregular caudal vertebrae fusion 9 . The observed ectopic neural tissue indicates that investigation of the development of individual tail structures may shed light on evolutionary changes in bird tail morphology.…”

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confidence: 99%

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Distal spinal nerve development and divergence of avian groups

Rashid¹,

Bradley²,

Bailleul³

et al. 2020

Sci Rep

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The avian transition from long to short, distally fused tails during the Mesozoic ushered in the Pygostylian group, which includes modern birds. The avian tail embodies a bipartite anatomy, with the proximal separate caudal vertebrae region, and the distal pygostyle, formed by vertebral fusion. This study investigates developmental features of the two tail domains in different bird groups, and analyzes them in reference to evolutionary origins. We first defined the early developmental boundary between the two tail halves in the chicken, then followed major developmental structures from early embryo to post-hatching stages. Differences between regions were observed in sclerotome anterior/posterior polarity and peripheral nervous system development, and these were consistent in other neognathous birds. However, in the paleognathous emu, the neognathous pattern was not observed, such that spinal nerve development extends through the pygostyle region. Disparities between the neognaths and paleognaths studied were also reflected in the morphology of their pygostyles. The ancestral long-tailed spinal nerve configuration was hypothesized from brown anole and alligator, which unexpectedly more resembles the neognathous birds. This study shows that tail anatomy is not universal in avians, and suggests several possible scenarios regarding bird evolution, including an independent paleognathous long-tailed ancestor. Vertebrate tails are highly divergent in form and function. In birds, tails have evolved adaptations specific for flight and sexual selection. Extant bird tails are composed of the proximal region, characterized by unfused ('free') caudal vertebrae, and the distal region harboring the pygostyle, a bony structure formed from fusion of the distal caudals. The observation that pygostyle fusion occurs progressively after hatching 1 led us to question how the unique avian tail morphology is rooted in early developmental events, and whether these events are consistent across all three major groups of extant birds (neoaves, galloanseriforms, and paleognaths). The modern bird tail originated in the Mesozoic era, at the long-to short-tailed transition 2. Archaeopteryx, the earliest known bird, sported a long, reptilian-like tail with greater than 20 caudal vertebrae 3,4. While Archaeopteryx fossil specimens were discovered in Germany, the greatest cache of Mesozoic bird fossils has been found in the Jehol beds in China, representing a period between 131 to 120 million years ago 5. Jehol specimens indicate that both long and short-tailed birds coexisted at this critical time in avian evolution. The short-tailed birds exhibited a number of unique morphologies, among them the occurrence of the pygostyle and additional bone fusions throughout the axial and peripheral skeleton 6. With the exception of Rahonavis, a specimen from Madagascar that may or may not have been avian 7 , in the last 120 million years, only short-tailed birds have been

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Section: Resultssupporting

confidence: 90%

Section: Development Of Structures In the Pygostyle And Free Vertebramentioning

confidence: 99%

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confidence: 99%

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Distal spinal nerve development and divergence of avian groups

Rashid¹,

Bradley²,

Bailleul³

et al. 2020

Sci Rep

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“…There is now strong evidence from several vertebrate species that paraxial mesoderm continues to be generated from bipotential neuromesodermal progenitors (NMPs) throughout the entire course of somite formation and axis extension (Fig. 1A, B) [3][4][5][6][7][8][9]. During commitment to 3 the mesodermal lineage from NMPs, cells exist in a niche (also referred to as the mesodermal maturation zone) that has defined molecular and cellular properties ( Fig.…”

Section: Introductionmentioning

confidence: 99%

Factors that coordinate mesoderm specification from neuromesodermal progenitors with segmentation during vertebrate axial extension

Martin

2016

Seminars in Cell & Developmental Biology

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The formation of the vertebrate body depends on the precise timing and coordination of molecular and morphological events. During vertebrate embryogenesis, the paraxial mesoderm is segmented into structures called somites in a progressive fashion from the anterior to the posterior at the same time as the entire body axis elongates in the posterior direction. Evidence from several vertebrate species indicates that new paraxial mesoderm is continuously induced from neuromesodermal progenitors at the posterior-most end of the embryo. The newly forming mesoderm exists in a specialized environment called the mesodermal progenitor niche. This review will discuss how the progenitor niche coordinates the continuous addition of new mesoderm to the body axis with proper segmentation of this mesoderm upon exit from the niche. I will focus on evidence that the t-box transcription factor Brachyury and its downstream transcriptional targets serve as the primary factors coordinating mesoderm specification with somitogenesis. I will end with a discussion of recent exciting work regarding the cell-cycle and migratory behavior of mesodermal cells as they exit the progenitor niche, which may serve to further integrate new mesoderm production with proper segmentation.

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“…Recent work demonstrated that the caudalmost progenitors within the tailbud, the posterior wall progenitor cells (PWPCs; sometimes referred to as neuromesodermal progenitors), are bipotential and continuously make neural/mesodermal fate decisions during embryo elongation. (Freese et al, 2014;Garriock et al, 2015;Gentsch et al, 2013;Gouti et al, 2014;Kondoh and Takemoto, 2012;Martin and Kimelman, 2012;Tzouanacou et al, 2009). These cells give rise to the growing spinal cord, somites and vasculature.…”

Section: Introductionmentioning

confidence: 99%

The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

et al. 2015

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Vertebrate body axis formation depends on a population of bipotential neuromesodermal cells along the posterior wall of the tailbud that make a germ layer decision after gastrulation to form spinal cord and mesoderm. Despite exhibiting germ layer plasticity, these cells never give rise to midline tissues of the notochord, floor plate and dorsal endoderm, raising the question of whether midline tissues also arise from basal posterior progenitors after gastrulation. We show in zebrafish that local posterior signals specify germ layer fate in two basal tailbud midline progenitor populations. Wnt signaling induces notochord within a population of notochord/floor plate bipotential cells through negative transcriptional regulation of sox2. Notch signaling, required for hypochord induction during gastrulation, continues to act in the tailbud to specify hypochord from a notochord/hypochord bipotential cell population. Our results lend strong support to a continuous allocation model of midline tissue formation in zebrafish, and provide an embryological basis for zebrafish and mouse bifurcated notochord phenotypes as well as the rare human congenital split notochord syndrome. We demonstrate developmental equivalency between the tailbud progenitor cell populations. Midline progenitors can be transfated from notochord to somite fate after gastrulation by ectopic expression of msgn1, a master regulator of paraxial mesoderm fate, or if transplanted into the bipotential progenitors that normally give rise to somites. Our results indicate that the entire non-epidermal posterior body is derived from discrete, basal tailbud cell populations. These cells remain receptive to extracellular cues after gastrulation and continue to make basic germ layer decisions.

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A Novel Gain-Of-Function Mutation of the Proneural IRX1 and IRX2 Genes Disrupts Axis Elongation in the Araucana Rumpless Chicken

Cited by 24 publications

References 88 publications

Distal spinal nerve development and divergence of avian groups

Distal spinal nerve development and divergence of avian groups

Factors that coordinate mesoderm specification from neuromesodermal progenitors with segmentation during vertebrate axial extension

The zebrafish tailbud contains two independent populations of midline progenitor cells that maintain long-term germ layer plasticity and differentiate based on local signaling cues

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