Size-reduced embryos reveal a gradient scaling-based mechanism for zebrafish somite formation
Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poor...
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Published in | Development (Cambridge) Vol. 145; no. 11; p. dev161257 |
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Main Authors | , , , , , , , , |
Format | Journal Article |
Language | English |
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The Company of Biologists Ltd
01.06.2018
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Abstract | Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poorly understood. Here, we examine somite scaling and find that somite size at specification scales with the length of the presomitic mesoderm (PSM) despite considerable variation in PSM length across developmental stages and in surgically size-reduced embryos. Measurement of clock period, axis elongation speed and clock gene expression patterns demonstrate that existing models fail to explain scaling. We posit a 'clock and scaled gradient' model, in which somite boundaries are set by a dynamically scaling signaling gradient across the PSM. Our model not only explains existing data, but also makes a unique prediction that we confirm experimentally - the formation of periodic 'echoes' in somite size following perturbation of the size of one somite. Our findings demonstrate that gradient scaling plays a central role in both progression and size control of somitogenesis. |
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AbstractList | Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poorly understood. Here we examine somite scaling and find that somite size at specification scales with the length of the presomitic mesoderm (PSM) despite considerable variation in PSM length across developmental stages and in surgically size-reduced embryos. Measurement of clock period, axis elongation speed, and clock gene expression patterns demonstrate that existing models fail to explain scaling. We posit a “clock and scaled gradient” model, in which somite boundaries are set by a dynamically scaling signaling gradient across the PSM. Our model not only explains existing data, but also makes a unique prediction that we experimentally confirm—the formation of periodic “echoes” in somite size following perturbation of the size of one somite. Our findings demonstrate that gradient scaling plays a central role both in progression and size control of somitogenesis. Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poorly understood. Here, we examine somite scaling and find that somite size at specification scales with the length of the presomitic mesoderm (PSM) despite considerable variation in PSM length across developmental stages and in surgically size-reduced embryos. Measurement of clock period, axis elongation speed and clock gene expression patterns demonstrate that existing models fail to explain scaling. We posit a ‘clock and scaled gradient’ model, in which somite boundaries are set by a dynamically scaling signaling gradient across the PSM. Our model not only explains existing data, but also makes a unique prediction that we confirm experimentally – the formation of periodic ‘echoes’ in somite size following perturbation of the size of one somite. Our findings demonstrate that gradient scaling plays a central role in both progression and size control of somitogenesis.Highlighted Article: A new ‘clock and scaled gradient’ model of zebrafish somite formation demonstrates that dynamic gradient scaling in the presomitic mesoderm plays a central role in progression and size control of somitogenesis. Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poorly understood. Here, we examine somite scaling and find that somite size at specification scales with the length of the presomitic mesoderm (PSM) despite considerable variation in PSM length across developmental stages and in surgically size-reduced embryos. Measurement of clock period, axis elongation speed and clock gene expression patterns demonstrate that existing models fail to explain scaling. We posit a 'clock and scaled gradient' model, in which somite boundaries are set by a dynamically scaling signaling gradient across the PSM. Our model not only explains existing data, but also makes a unique prediction that we confirm experimentally - the formation of periodic 'echoes' in somite size following perturbation of the size of one somite. Our findings demonstrate that gradient scaling plays a central role in both progression and size control of somitogenesis. Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and across species. Despite intense study of the segmentation clock governing the timing of somite generation, how it relates to somite size is poorly understood. Here, we examine somite scaling and find that somite size at specification scales with the length of the presomitic mesoderm (PSM) despite considerable variation in PSM length across developmental stages and in surgically size-reduced embryos. Measurement of clock period, axis elongation speed and clock gene expression patterns demonstrate that existing models fail to explain scaling. We posit a ‘clock and scaled gradient’ model, in which somite boundaries are set by a dynamically scaling signaling gradient across the PSM. Our model not only explains existing data, but also makes a unique prediction that we confirm experimentally – the formation of periodic ‘echoes’ in somite size following perturbation of the size of one somite. Our findings demonstrate that gradient scaling plays a central role in both progression and size control of somitogenesis. Highlighted Article: A new ‘clock and scaled gradient’ model of zebrafish somite formation demonstrates that dynamic gradient scaling in the presomitic mesoderm plays a central role in progression and size control of somitogenesis. |
Author | Collins, Zach M Matsui, Takaaki Hiscock, Tom W Richmond, David L Sari, Dini Wahyu Kartika Megason, Sean G Ishimatsu, Kana Bessho, Yasumasa Lischer, Kenny |
AuthorAffiliation | 3 Department of Fisheries , Universitas Gadjah Mada , Yogyakarta 55281 , Indonesia 2 Gene Regulation Research, Nara Institute of Science and Technology , Nara 630-0101 , Japan 4 Image and Data Analysis Core, Harvard Medical School , Boston, MA 02115 , USA 1 Department of Systems Biology , Harvard Medical School , Boston, MA 02115 , USA |
AuthorAffiliation_xml | – name: 3 Department of Fisheries , Universitas Gadjah Mada , Yogyakarta 55281 , Indonesia – name: 4 Image and Data Analysis Core, Harvard Medical School , Boston, MA 02115 , USA – name: 1 Department of Systems Biology , Harvard Medical School , Boston, MA 02115 , USA – name: 2 Gene Regulation Research, Nara Institute of Science and Technology , Nara 630-0101 , Japan |
Author_xml | – sequence: 1 givenname: Kana orcidid: 0000-0002-4434-0088 surname: Ishimatsu fullname: Ishimatsu, Kana email: kana_ishimatsu@hms.harvard.edu, megason@hms.harvard.edu organization: Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA kana_ishimatsu@hms.harvard.edu megason@hms.harvard.edu – sequence: 2 givenname: Tom W surname: Hiscock fullname: Hiscock, Tom W organization: Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 3 givenname: Zach M surname: Collins fullname: Collins, Zach M organization: Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 4 givenname: Dini Wahyu Kartika surname: Sari fullname: Sari, Dini Wahyu Kartika organization: Department of Fisheries, Universitas Gadjah Mada, Yogyakarta 55281, Indonesia – sequence: 5 givenname: Kenny surname: Lischer fullname: Lischer, Kenny organization: Gene Regulation Research, Nara Institute of Science and Technology, Nara 630-0101, Japan – sequence: 6 givenname: David L surname: Richmond fullname: Richmond, David L organization: Image and Data Analysis Core, Harvard Medical School, Boston, MA 02115, USA – sequence: 7 givenname: Yasumasa surname: Bessho fullname: Bessho, Yasumasa organization: Gene Regulation Research, Nara Institute of Science and Technology, Nara 630-0101, Japan – sequence: 8 givenname: Takaaki surname: Matsui fullname: Matsui, Takaaki organization: Gene Regulation Research, Nara Institute of Science and Technology, Nara 630-0101, Japan – sequence: 9 givenname: Sean G orcidid: 0000-0002-9330-2934 surname: Megason fullname: Megason, Sean G email: kana_ishimatsu@hms.harvard.edu, megason@hms.harvard.edu organization: Department of Systems Biology, Harvard Medical School, Boston, MA 02115, USA kana_ishimatsu@hms.harvard.edu megason@hms.harvard.edu |
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Keywords | Somite Scaling Zebrafish Mathematical modeling Quantitative imaging Fgf gradient PSM Segmentation clock |
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Snippet | Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size, which varies widely both within an individual and... Little is known about how the sizes of animal tissues are controlled. A prominent example is somite size which varies widely both within an individual and... |
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SubjectTerms | Animals Basic Helix-Loop-Helix Transcription Factors - physiology Body Patterning - genetics Body Size - physiology Cleavage Stage, Ovum - physiology Clock gene Danio rerio Developmental stages Embryos Fibroblast Growth Factors - metabolism Gene expression Gene Expression Regulation, Developmental - genetics Mesoderm Models, Theoretical Morphogenesis - genetics Organ Size - physiology Scaling Segmentation Somites - embryology Somitogenesis Zebrafish - embryology Zebrafish Proteins - physiology |
Title | Size-reduced embryos reveal a gradient scaling-based mechanism for zebrafish somite formation |
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