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Segmentation clock gene pairing drives robust pattern formation

Gene expression is an inherently stochastic process (1,2); however, organismal development and homeostasis require that cells spatiotemporally coordinate the expression of large sets of genes. Coexpressed gene pairs in metazoans often reside in the same chromosomal neighborhood, with gene pairs repr...

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Autores principales: Zinani, Oriana Q.H., Keseroğlu, Kemal, Ay, Ahmet, Özbudak, Ertuğrul M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7932681/
https://www.ncbi.nlm.nih.gov/pubmed/33361814
http://dx.doi.org/10.1038/s41586-020-03055-0
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author Zinani, Oriana Q.H.
Keseroğlu, Kemal
Ay, Ahmet
Özbudak, Ertuğrul M.
author_facet Zinani, Oriana Q.H.
Keseroğlu, Kemal
Ay, Ahmet
Özbudak, Ertuğrul M.
author_sort Zinani, Oriana Q.H.
collection PubMed
description Gene expression is an inherently stochastic process (1,2); however, organismal development and homeostasis require that cells spatiotemporally coordinate the expression of large sets of genes. Coexpressed gene pairs in metazoans often reside in the same chromosomal neighborhood, with gene pairs representing 10% - 50% of all genes depending on species (3–6). As shared upstream regulators can ensure correlated gene expression, the selective advantage of maintaining adjacent gene pairs remains unknown (6). Here, using two linked zebrafish segmentation clock genes, her1 and her7, and combining single-cell transcript counting, genetic engineering, real-time imaging and computational modeling, we reveal that gene pairing boosts correlated transcription and provides phenotypic robustness for developmental pattern formation. Our results demonstrate that disrupting gene pairing disrupts oscillations and segmentation, identifying the selective pressure retaining correlated transcription to sustain a robust and rapid developmental clock. We anticipate that these findings will inspire investigating advantages of gene pairing in other systems and engineering precise synthetic clocks in embryos and organoids.
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spelling pubmed-79326812021-06-23 Segmentation clock gene pairing drives robust pattern formation Zinani, Oriana Q.H. Keseroğlu, Kemal Ay, Ahmet Özbudak, Ertuğrul M. Nature Article Gene expression is an inherently stochastic process (1,2); however, organismal development and homeostasis require that cells spatiotemporally coordinate the expression of large sets of genes. Coexpressed gene pairs in metazoans often reside in the same chromosomal neighborhood, with gene pairs representing 10% - 50% of all genes depending on species (3–6). As shared upstream regulators can ensure correlated gene expression, the selective advantage of maintaining adjacent gene pairs remains unknown (6). Here, using two linked zebrafish segmentation clock genes, her1 and her7, and combining single-cell transcript counting, genetic engineering, real-time imaging and computational modeling, we reveal that gene pairing boosts correlated transcription and provides phenotypic robustness for developmental pattern formation. Our results demonstrate that disrupting gene pairing disrupts oscillations and segmentation, identifying the selective pressure retaining correlated transcription to sustain a robust and rapid developmental clock. We anticipate that these findings will inspire investigating advantages of gene pairing in other systems and engineering precise synthetic clocks in embryos and organoids. 2020-12-23 2021-01 /pmc/articles/PMC7932681/ /pubmed/33361814 http://dx.doi.org/10.1038/s41586-020-03055-0 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms Reprints and permissions information is available at http://www.nature.com/reprints.
spellingShingle Article
Zinani, Oriana Q.H.
Keseroğlu, Kemal
Ay, Ahmet
Özbudak, Ertuğrul M.
Segmentation clock gene pairing drives robust pattern formation
title Segmentation clock gene pairing drives robust pattern formation
title_full Segmentation clock gene pairing drives robust pattern formation
title_fullStr Segmentation clock gene pairing drives robust pattern formation
title_full_unstemmed Segmentation clock gene pairing drives robust pattern formation
title_short Segmentation clock gene pairing drives robust pattern formation
title_sort segmentation clock gene pairing drives robust pattern formation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7932681/
https://www.ncbi.nlm.nih.gov/pubmed/33361814
http://dx.doi.org/10.1038/s41586-020-03055-0
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