Multiple morphogens and rapid elongation promote segmental patterning during development.

The vertebrate hindbrain is segmented into rhombomeres (r) initially defined by distinct domains of gene expression. Previous studies have shown that noise-induced gene regulation and cell sorting are critical for the sharpening of rhombomere boundaries, which start out rough in the forming neural p...

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Autores principales:	Yuchi Qiu, Lianna Fung, Thomas F Schilling, Qing Nie
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/70871c8fd7b74d20bbcd554b7a7ddeca
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spelling	oai:doaj.org-article:70871c8fd7b74d20bbcd554b7a7ddeca2021-11-25T05:40:35ZMultiple morphogens and rapid elongation promote segmental patterning during development.1553-734X1553-735810.1371/journal.pcbi.1009077https://doaj.org/article/70871c8fd7b74d20bbcd554b7a7ddeca2021-06-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009077https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358The vertebrate hindbrain is segmented into rhombomeres (r) initially defined by distinct domains of gene expression. Previous studies have shown that noise-induced gene regulation and cell sorting are critical for the sharpening of rhombomere boundaries, which start out rough in the forming neural plate (NP) and sharpen over time. However, the mechanisms controlling simultaneous formation of multiple rhombomeres and accuracy in their sizes are unclear. We have developed a stochastic multiscale cell-based model that explicitly incorporates dynamic morphogenetic changes (i.e. convergent-extension of the NP), multiple morphogens, and gene regulatory networks to investigate the formation of rhombomeres and their corresponding boundaries in the zebrafish hindbrain. During pattern initiation, the short-range signal, fibroblast growth factor (FGF), works together with the longer-range morphogen, retinoic acid (RA), to specify all of these boundaries and maintain accurately sized segments with sharp boundaries. At later stages of patterning, we show a nonlinear change in the shape of rhombomeres with rapid left-right narrowing of the NP followed by slower dynamics. Rapid initial convergence improves boundary sharpness and segment size by regulating cell sorting and cell fate both independently and coordinately. Overall, multiple morphogens and tissue dynamics synergize to regulate the sizes and boundaries of multiple segments during development.Yuchi QiuLianna FungThomas F SchillingQing NiePublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 6, p e1009077 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Yuchi Qiu Lianna Fung Thomas F Schilling Qing Nie Multiple morphogens and rapid elongation promote segmental patterning during development.
description	The vertebrate hindbrain is segmented into rhombomeres (r) initially defined by distinct domains of gene expression. Previous studies have shown that noise-induced gene regulation and cell sorting are critical for the sharpening of rhombomere boundaries, which start out rough in the forming neural plate (NP) and sharpen over time. However, the mechanisms controlling simultaneous formation of multiple rhombomeres and accuracy in their sizes are unclear. We have developed a stochastic multiscale cell-based model that explicitly incorporates dynamic morphogenetic changes (i.e. convergent-extension of the NP), multiple morphogens, and gene regulatory networks to investigate the formation of rhombomeres and their corresponding boundaries in the zebrafish hindbrain. During pattern initiation, the short-range signal, fibroblast growth factor (FGF), works together with the longer-range morphogen, retinoic acid (RA), to specify all of these boundaries and maintain accurately sized segments with sharp boundaries. At later stages of patterning, we show a nonlinear change in the shape of rhombomeres with rapid left-right narrowing of the NP followed by slower dynamics. Rapid initial convergence improves boundary sharpness and segment size by regulating cell sorting and cell fate both independently and coordinately. Overall, multiple morphogens and tissue dynamics synergize to regulate the sizes and boundaries of multiple segments during development.
format	article
author	Yuchi Qiu Lianna Fung Thomas F Schilling Qing Nie
author_facet	Yuchi Qiu Lianna Fung Thomas F Schilling Qing Nie
author_sort	Yuchi Qiu
title	Multiple morphogens and rapid elongation promote segmental patterning during development.
title_short	Multiple morphogens and rapid elongation promote segmental patterning during development.
title_full	Multiple morphogens and rapid elongation promote segmental patterning during development.
title_fullStr	Multiple morphogens and rapid elongation promote segmental patterning during development.
title_full_unstemmed	Multiple morphogens and rapid elongation promote segmental patterning during development.
title_sort	multiple morphogens and rapid elongation promote segmental patterning during development.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/70871c8fd7b74d20bbcd554b7a7ddeca
work_keys_str_mv	AT yuchiqiu multiplemorphogensandrapidelongationpromotesegmentalpatterningduringdevelopment AT liannafung multiplemorphogensandrapidelongationpromotesegmentalpatterningduringdevelopment AT thomasfschilling multiplemorphogensandrapidelongationpromotesegmentalpatterningduringdevelopment AT qingnie multiplemorphogensandrapidelongationpromotesegmentalpatterningduringdevelopment
_version_	1718414523657879552

Multiple morphogens and rapid elongation promote segmental patterning during development.

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