Symmetry breaking in the embryonic skin triggers a directional and sequential front of competence during plumage patterning
Preprint posted on 8 December 2018 https://www.biorxiv.org/content/early/2018/12/08/491092
Article now published in PLOS Biology at http://dx.doi.org/10.1371/journal.pbio.3000448
Feathers set the bar to study pattern formation: wonderful work combining a unified model and experimental data to recapitulate the complex sequence of events of plumage patterning #modeling #devbio #evodevo #preprint
Selected by Alexa Sadier
Categories: developmental biology, evolutionary biology, systems biology
Background
One of the key challenges of developmental biology is to explain how patterns arise and develop from a homogenous structure (such as skin) to give rise to complex organs (such as feathers) in a robust and reproducible manner. Research in the past few decades has revealed that patterning is a complex combination of differential gene expression, morphogenetic movements and mechano-chemical processes. As a result, modelling the establishment of a pattern from the beginning to the end has been challenging and most models consist of reproducing the final states of patterning events (e.g. spacing of hair, feather or teeth). In addition, these models are often limited to particular cases and are not able to explain how the diversity of motifs seen in nature can arise from pattern formation. To tackle this question, Bailleul and colleagues chose the example of bird plumage, looking at the patterning of tracts in which feathers are inserted. The interest of this choice is twofold. First, the events at the origin of feather tract patterning are well established in chicken, which allows its study from a modelling point of view with a good knowledge of the underlying mechanisms. Second, tracts and feathers are highly variable in terms of size, shape, number and pattern of emergence among species. For these reasons, the plumage of birds constitutes a perfect example to study these mechanisms and their variations.
Key findings
To build a realistic model that can explain both shared and variable mechanisms responsible for feather tract patterning, the authors first established the expression pattern of β-catenin transcript that is known to mark the early differentiation of feather follicles, in five different representative species of birds. This pattern of expression revealed the temporal dynamics of emergence of feather tracts and the pre-patterning events that initiate the lateral and sequential addition of new feathers in all the five species.
To identify the key parameters influencing tract patterning, the authors tested several classical patterning models separately. These models, such as classical reaction-diffusion mechanisms, chemotaxis or cell proliferation-based models, can each produce a pattern but fail to reproduce the pre-patterning and/or the sequential/directional addition of tracts rows, showing that multiple mechanisms are involved in the patterning process. To resolve this issue, they built a unified model combining these characteristics and tested it for each species or bird. Remarkably, simulations of this model based on a unique set of parameters for all the species, but with species-specific initial conditions, were able to recapitulate the formation of tracts in a bi-directional, row-by-row manner and with a realistic duration for all the five species of birds.
Then, they used this model to identify the events at the origin of the initial conditions observed in the different species. The resulting simulations revealed that the directional and sequential progression of tract differentiation results from a pre-pattern, and that this progression is due to a traveling front of increased cell density that defines the domains with self-organizing capacity.
Finally, the authors demonstrated the importance of cell proliferation, predicted by the model, for the duration of the patterning process by performing ex and in vivo experiments using BrdU or colchicine (which respectively labels and blocks cell proliferation). Altogether, these simulations and experimental results led to propose a complete scenario to explain the complex patterning of feather tracts and the origin of its variation in different species.
Why this work is important
This preprint sets the bar concerning the level of modelling and experimental data needed to completely describe pattern formation. While a lot of models consist of reproducing a snapshot of the final stage of a pattern, this one is able to recapitulate precisely all the steps of pattern formation, their dynamics and their duration.
Another important point of this preprint is the strength of the model that is able to reproduce accurately some key features of pattern formation, such as the temporal sequence, without resort to external forcing. The result is a unified and robust model that can be tuned and adapted to different scenarios, species and potentially other organs.
More broadly, this preprint fills a gap in our understanding of how repeated patterns are established and can be both extremely stable while allowing some variation in different species. This work is likely to be extended to other ectodermal appendages (for example: hair, scales, teeth, external glands or nails) and, to a certain extent, other replicated structures.
Future directions and questions for the authors
- To what extent can this model be applied to other ectodermal appendages or, more broadly, repeated structures, that are known to share common patterning mechanisms?
- Do you think that this model and the underlying developmental mechanisms constitute a developmental bias that constrains feather/ectodermal appendages evolution?
- Aside from classical feather GRNs genes such as Wnt, Eda or Shh, do you expect cell proliferation genes or other factors to be involved in pattern formation and evolution?
Additional references
- Kondo, S. & Miura, T. Reaction Diffusion as a framework for understanding biological pattern formation. Science 329, 1616-1620 (2010)
- Painter,K.J., Hunt, G., Wells, K., Johanneson, K. & Headon, D.J. Towards an integrated experimental–theoretical approach for assessing the mechanistic basis of hair and feather morphogenesis. Interface Focus 2, 433-450 (2012)
- Painter, K.J., Ho, W. & Headon, D.J. A chemotaxis model of feather primordia pattern formation during avian development. Journal of Theoretical Biology 437, 225-238 (2018)
Posted on: 21 December 2018
doi: https://doi.org/10.1242/prelights.6754
Read preprint
(No Ratings Yet)Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the developmental biology category:
Temporal constraints on enhancer usage shape the regulation of limb gene transcription
OGT prevents DNA demethylation and suppresses the expression of transposable elements in heterochromatin by restraining TET activity genome-wide
Actin polymerization drives lumen formation in a human epiblast model
Also in the evolutionary biology category:
A long non-coding RNA at the cortex locus controls adaptive colouration in butterflies
AND
The ivory lncRNA regulates seasonal color patterns in buckeye butterflies
AND
A micro-RNA drives a 100-million-year adaptive evolution of melanic patterns in butterflies and moths
A complex Plasmodium falciparum cryptotype circulating at low frequency across the African continent
Evolution of tandem repeats in putative CSP to enhance its function: A recent and exclusive event in Plasmodium vivax in India
Also in the systems biology category:
Expressive modeling and fast simulation for dynamic compartments
Clusters of lineage-specific genes are anchored by ZNF274 in repressive perinucleolar compartments
Holimap: an accurate and efficient method for solving stochastic gene network dynamics
preLists in the developmental biology category:
GfE/ DSDB meeting 2024
This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.
| List by | Joyce Yu |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
preLights peer support – preprints of interest
This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.
| List by | preLights peer support |
The Society for Developmental Biology 82nd Annual Meeting
This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.
| List by | Joyce Yu, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
| List by | Helen Zenner |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
| List by | Nándor Lipták |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
Society for Developmental Biology 79th Annual Meeting
Preprints at SDB 2020
| List by | Irepan Salvador-Martinez, Martin Estermann |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
| List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
| List by | Paul Gerald L. Sanchez and Stefano Vianello |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EDBC Alicante 2019
Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.
| List by | Sergio Menchero et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
Young Embryologist Network Conference 2019
Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
| List by | Dey Lab |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
| List by | Shikha Nayar |
Also in the evolutionary biology category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
preLights peer support – preprints of interest
This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.
| List by | preLights peer support |
EMBO | EMBL Symposium: The organism and its environment
This preList contains preprints discussed during the 'EMBO | EMBL Symposium: The organism and its environment', organised at EMBL Heidelberg, Germany (May 2023).
| List by | Girish Kale |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
| List by | Dey Lab, Zhang-He Goh |
1
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |
Also in the systems biology category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Single Cell Biology 2020
A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.
| List by | Alex Eve |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |