Self-organized BMP signaling dynamics underlie the development and evolution of digit segmentation patterns in birds and mammals Article Swipe
Emmanuelle Grall
,
Christian Feregrino
,
Sabrina Fischer
,
Aline De Courten
,
Fabio Sacher
,
Tom W. Hiscock
,
Patrick Tschopp
·
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1073/pnas.2304470121
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1073/pnas.2304470121
Repeating patterns of synovial joints are a highly conserved feature of articulated digits, with variations in joint number and location resulting in diverse digit morphologies and limb functions across the tetrapod clade. During the development of the amniote limb, joints form iteratively within the growing digit ray, as a population of distal progenitors alternately specifies joint and phalanx cell fates to segment the digit into distinct elements. While numerous molecular pathways have been implicated in this fate choice, it remains unclear how they give rise to a repeating pattern. Here, using single-cell RNA sequencing and spatial gene expression profiling, we investigate the transcriptional dynamics of interphalangeal joint specification in vivo. Combined with mathematical modeling, we predict that interactions within the BMP signaling pathway—between the ligand GDF5, the inhibitor NOGGIN, and the intracellular effector pSMAD—result in a self-organizing Turing system that forms periodic joint patterns. Our model is able to recapitulate the spatiotemporal gene expression dynamics observed in vivo, as well as phenocopy digit malformations caused by BMP pathway perturbations. By contrasting in silico simulations with in vivo morphometrics of two morphologically distinct digits, we show how changes in signaling parameters and growth dynamics can result in variations in the size and number of phalanges. Together, our results reveal a self-organizing mechanism that underpins amniote digit segmentation and its evolvability and, more broadly, illustrate how Turing systems based on a single molecular pathway may generate complex repetitive patterns in a wide variety of organisms.
Related Topics
Concepts
Biology
Amniote
Hox gene
Homeotic gene
Numerical digit
Limb development
Developmental biology
Evolutionary biology
Genetics
Vertebrate
Gene
Gene expression
Arithmetic
Mathematics
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1073/pnas.2304470121
- https://www.pnas.org/doi/pdf/10.1073/pnas.2304470121
- OA Status
- hybrid
- Cited By
- 15
- References
- 89
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4390578011
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4390578011Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1073/pnas.2304470121Digital Object Identifier
- Title
-
Self-organized BMP signaling dynamics underlie the development and evolution of digit segmentation patterns in birds and mammalsWork title
- Type
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articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2024Year of publication
- Publication date
-
2024-01-04Full publication date if available
- Authors
-
Emmanuelle Grall, Christian Feregrino, Sabrina Fischer, Aline De Courten, Fabio Sacher, Tom W. Hiscock, Patrick TschoppList of authors in order
- Landing page
-
https://doi.org/10.1073/pnas.2304470121Publisher landing page
- PDF URL
-
https://www.pnas.org/doi/pdf/10.1073/pnas.2304470121Direct link to full text PDF
- Open access
-
YesWhether a free full text is available
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hybridOpen access status per OpenAlex
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https://www.pnas.org/doi/pdf/10.1073/pnas.2304470121Direct OA link when available
- Concepts
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Biology, Amniote, Hox gene, Homeotic gene, Numerical digit, Limb development, Developmental biology, Evolutionary biology, Genetics, Vertebrate, Gene, Gene expression, Arithmetic, MathematicsTop concepts (fields/topics) attached by OpenAlex
- Cited by
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15Total citation count in OpenAlex
- Citations by year (recent)
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2025: 10, 2024: 5Per-year citation counts (last 5 years)
- References (count)
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89Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| cited_by_percentile_year.min | 98 |
| corresponding_author_ids | https://openalex.org/A5026934867, https://openalex.org/A5029188385 |
| countries_distinct_count | 2 |
| institutions_distinct_count | 7 |
| corresponding_institution_ids | https://openalex.org/I1850255, https://openalex.org/I195460627 |
| sustainable_development_goals[0].id | https://metadata.un.org/sdg/15 |
| sustainable_development_goals[0].score | 0.550000011920929 |
| sustainable_development_goals[0].display_name | Life in Land |
| citation_normalized_percentile.value | 0.95483137 |
| citation_normalized_percentile.is_in_top_1_percent | False |
| citation_normalized_percentile.is_in_top_10_percent | True |