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Mechanical Coupling between Endoderm Invagination and Axis Extension in Drosophila.

Lye CM, Blanchard GB, Naylor HW, Muresan L, Huisken J, Adams RJ, Sanson B - PLoS Biol. (2015)

Bottom Line: We found previously that cells elongate in the anteroposterior (AP) axis in the extending germband, suggesting that an extrinsic tensile force contributed to body axis extension.We next looked for evidence of this force in a simplified system without polarized cell intercalation, in acellular embryos.This highlights the importance of physical interactions between tissues during morphogenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
How genetic programs generate cell-intrinsic forces to shape embryos is actively studied, but less so how tissue-scale physical forces impact morphogenesis. Here we address the role of the latter during axis extension, using Drosophila germband extension (GBE) as a model. We found previously that cells elongate in the anteroposterior (AP) axis in the extending germband, suggesting that an extrinsic tensile force contributed to body axis extension. Here we further characterized the AP cell elongation patterns during GBE, by tracking cells and quantifying their apical cell deformation over time. AP cell elongation forms a gradient culminating at the posterior of the embryo, consistent with an AP-oriented tensile force propagating from there. To identify the morphogenetic movements that could be the source of this extrinsic force, we mapped gastrulation movements temporally using light sheet microscopy to image whole Drosophila embryos. We found that both mesoderm and endoderm invaginations are synchronous with the onset of GBE. The AP cell elongation gradient remains when mesoderm invagination is blocked but is abolished in the absence of endoderm invagination. This suggested that endoderm invagination is the source of the tensile force. We next looked for evidence of this force in a simplified system without polarized cell intercalation, in acellular embryos. Using Particle Image Velocimetry, we identify posteriorwards Myosin II flows towards the presumptive posterior endoderm, which still undergoes apical constriction in acellular embryos as in wildtype. We probed this posterior region using laser ablation and showed that tension is increased in the AP orientation, compared to dorsoventral orientation or to either orientations more anteriorly in the embryo. We propose that apical constriction leading to endoderm invagination is the source of the extrinsic force contributing to germband extension. This highlights the importance of physical interactions between tissues during morphogenesis.

No MeSH data available.


Related in: MedlinePlus

AP cell elongation patterns form an AP gradient.(A, B) AP cell length change shown for each analyzed cell, for timepoints 7.5, 10, and 12.5 min after GBE onset in anterior (A, wtLB009) and posterior views (B, wtCL051010). The color of the dot at the center of each cell corresponds to the scale bar shown. (A’, B’) Spatial maps summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of the position of cells in the AP (x-axis) and DV (y-axis) embryonic axes, for anterior (A’) and posterior views (B’) (average for five and four embryos per views, respectively). (C, D) Graphs summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of cell position in the AP axis, for anterior (C) and posterior views (D). (E) Graphs summarizing AP cell length change (y-axis), at 2.5, 5, and 7.5 min after the onset of GBE, as a function of cell position in the AP axis (x-axis) for posterior views (average for four wild-type embryos). The ribbon’s width shows the standard error (see Materials and Methods). Data associated with this figure can be found in S2 Data.
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pbio.1002292.g002: AP cell elongation patterns form an AP gradient.(A, B) AP cell length change shown for each analyzed cell, for timepoints 7.5, 10, and 12.5 min after GBE onset in anterior (A, wtLB009) and posterior views (B, wtCL051010). The color of the dot at the center of each cell corresponds to the scale bar shown. (A’, B’) Spatial maps summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of the position of cells in the AP (x-axis) and DV (y-axis) embryonic axes, for anterior (A’) and posterior views (B’) (average for five and four embryos per views, respectively). (C, D) Graphs summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of cell position in the AP axis, for anterior (C) and posterior views (D). (E) Graphs summarizing AP cell length change (y-axis), at 2.5, 5, and 7.5 min after the onset of GBE, as a function of cell position in the AP axis (x-axis) for posterior views (average for four wild-type embryos). The ribbon’s width shows the standard error (see Materials and Methods). Data associated with this figure can be found in S2 Data.

Mentions: The AP cell elongation patterns appeared to form a gradient increasing from the anterior to the posterior. To ascertain this, we examined a short period around the peak of AP cell elongation, from 7.5 min to 12.5 min after GBE onset (Fig 2). This confirmed that AP cell elongation increased steeply towards the posterior of the embryo (Fig 2A–2D), forming a gradient over a distance of about 150 μm in posterior views (average for four movies, Fig 2D). Although the gradient is clearest in posterior views, some AP gradation was already detectable in anterior views (average for five movies, Fig 2C), consistent with the notion that we are visualizing the beginning of the gradient in anterior views. In posterior views, we also looked at snapshots of the gradient earlier in GBE, at 2.5, 5, and 7.5 min: the gradient was at first shallow and confined to the more posterior part of the field of view; it then expanded towards the anterior and became steeper with time (Fig 2E). These results suggested that a tensile stress deformed the tissue from a posterior source, starting at the onset of GBE and propagating towards the anterior of the embryo over time.


Mechanical Coupling between Endoderm Invagination and Axis Extension in Drosophila.

Lye CM, Blanchard GB, Naylor HW, Muresan L, Huisken J, Adams RJ, Sanson B - PLoS Biol. (2015)

AP cell elongation patterns form an AP gradient.(A, B) AP cell length change shown for each analyzed cell, for timepoints 7.5, 10, and 12.5 min after GBE onset in anterior (A, wtLB009) and posterior views (B, wtCL051010). The color of the dot at the center of each cell corresponds to the scale bar shown. (A’, B’) Spatial maps summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of the position of cells in the AP (x-axis) and DV (y-axis) embryonic axes, for anterior (A’) and posterior views (B’) (average for five and four embryos per views, respectively). (C, D) Graphs summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of cell position in the AP axis, for anterior (C) and posterior views (D). (E) Graphs summarizing AP cell length change (y-axis), at 2.5, 5, and 7.5 min after the onset of GBE, as a function of cell position in the AP axis (x-axis) for posterior views (average for four wild-type embryos). The ribbon’s width shows the standard error (see Materials and Methods). Data associated with this figure can be found in S2 Data.
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Related In: Results  -  Collection

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pbio.1002292.g002: AP cell elongation patterns form an AP gradient.(A, B) AP cell length change shown for each analyzed cell, for timepoints 7.5, 10, and 12.5 min after GBE onset in anterior (A, wtLB009) and posterior views (B, wtCL051010). The color of the dot at the center of each cell corresponds to the scale bar shown. (A’, B’) Spatial maps summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of the position of cells in the AP (x-axis) and DV (y-axis) embryonic axes, for anterior (A’) and posterior views (B’) (average for five and four embryos per views, respectively). (C, D) Graphs summarizing AP cell length change over the 7.5–12.5 min time interval, as a function of cell position in the AP axis, for anterior (C) and posterior views (D). (E) Graphs summarizing AP cell length change (y-axis), at 2.5, 5, and 7.5 min after the onset of GBE, as a function of cell position in the AP axis (x-axis) for posterior views (average for four wild-type embryos). The ribbon’s width shows the standard error (see Materials and Methods). Data associated with this figure can be found in S2 Data.
Mentions: The AP cell elongation patterns appeared to form a gradient increasing from the anterior to the posterior. To ascertain this, we examined a short period around the peak of AP cell elongation, from 7.5 min to 12.5 min after GBE onset (Fig 2). This confirmed that AP cell elongation increased steeply towards the posterior of the embryo (Fig 2A–2D), forming a gradient over a distance of about 150 μm in posterior views (average for four movies, Fig 2D). Although the gradient is clearest in posterior views, some AP gradation was already detectable in anterior views (average for five movies, Fig 2C), consistent with the notion that we are visualizing the beginning of the gradient in anterior views. In posterior views, we also looked at snapshots of the gradient earlier in GBE, at 2.5, 5, and 7.5 min: the gradient was at first shallow and confined to the more posterior part of the field of view; it then expanded towards the anterior and became steeper with time (Fig 2E). These results suggested that a tensile stress deformed the tissue from a posterior source, starting at the onset of GBE and propagating towards the anterior of the embryo over time.

Bottom Line: We found previously that cells elongate in the anteroposterior (AP) axis in the extending germband, suggesting that an extrinsic tensile force contributed to body axis extension.We next looked for evidence of this force in a simplified system without polarized cell intercalation, in acellular embryos.This highlights the importance of physical interactions between tissues during morphogenesis.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom.

ABSTRACT
How genetic programs generate cell-intrinsic forces to shape embryos is actively studied, but less so how tissue-scale physical forces impact morphogenesis. Here we address the role of the latter during axis extension, using Drosophila germband extension (GBE) as a model. We found previously that cells elongate in the anteroposterior (AP) axis in the extending germband, suggesting that an extrinsic tensile force contributed to body axis extension. Here we further characterized the AP cell elongation patterns during GBE, by tracking cells and quantifying their apical cell deformation over time. AP cell elongation forms a gradient culminating at the posterior of the embryo, consistent with an AP-oriented tensile force propagating from there. To identify the morphogenetic movements that could be the source of this extrinsic force, we mapped gastrulation movements temporally using light sheet microscopy to image whole Drosophila embryos. We found that both mesoderm and endoderm invaginations are synchronous with the onset of GBE. The AP cell elongation gradient remains when mesoderm invagination is blocked but is abolished in the absence of endoderm invagination. This suggested that endoderm invagination is the source of the tensile force. We next looked for evidence of this force in a simplified system without polarized cell intercalation, in acellular embryos. Using Particle Image Velocimetry, we identify posteriorwards Myosin II flows towards the presumptive posterior endoderm, which still undergoes apical constriction in acellular embryos as in wildtype. We probed this posterior region using laser ablation and showed that tension is increased in the AP orientation, compared to dorsoventral orientation or to either orientations more anteriorly in the embryo. We propose that apical constriction leading to endoderm invagination is the source of the extrinsic force contributing to germband extension. This highlights the importance of physical interactions between tissues during morphogenesis.

No MeSH data available.


Related in: MedlinePlus