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 inDevelopment (Cambridge) Vol. 145; no. 11; p. dev161257
Main Authors Ishimatsu, Kana, Hiscock, Tom W, Collins, Zach M, Sari, Dini Wahyu Kartika, Lischer, Kenny, Richmond, David L, Bessho, Yasumasa, Matsui, Takaaki, Megason, Sean G
Format Journal Article
LanguageEnglish
Published England 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.
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
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  orcidid: 0000-0002-9330-2934
  surname: Megason
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  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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Issue 11
Keywords Somite
Scaling
Zebrafish
Mathematical modeling
Quantitative imaging
Fgf gradient
PSM
Segmentation clock
Language English
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SSID ssj0003677
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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...
SourceID pubmedcentral
proquest
crossref
pubmed
SourceType Open Access Repository
Aggregation Database
Index Database
StartPage dev161257
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
URI https://www.ncbi.nlm.nih.gov/pubmed/29769221
https://www.proquest.com/docview/2054084042
https://search.proquest.com/docview/2040763883
https://pubmed.ncbi.nlm.nih.gov/PMC6031319
Volume 145
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