TY - JOUR
T1 - Deconstructing gastrulation at single-cell resolution
AU - Stern, Tomer
AU - Shvartsman, Stanislav Y.
AU - Wieschaus, Eric F.
N1 - Funding Information:
We are grateful to Lucy Reading-Ikkanda for graphic design of the figures; Lisa Brown (Simons Foundation) for fruitful discussions on image processing; Trudi Schüpbach, Matej Krajnc (Jožef Stefan Institute), David Denberg, Tal Galili, and Yosi Keller (Bar-Ilan University) for fruitful discussions; Benny Shilo (Weizmann Institute of Science) for comments on the manuscript; Matthew Cahn (Princeton University) and the IT of Simons Foundation for technical support with computing resources; Reba Samantha and Laisa Eimont for bureaucratic assistance and Heping Jiang for stock maintenance; and lastly the Wieschaus and Shvartsman lab members for continuous support. The research was supported by the European Molecular Biology Organization long-term fellowship ALTF 215-2017 to T.S., the MCB 1516970 award from the NSF to S.Y.S., and the Howard Hughes Medical Institute to E.F.W.
Funding Information:
We are grateful to Lucy Reading-Ikkanda for graphic design of the figures; Lisa Brown (Simons Foundation) for fruitful discussions on image processing; Trudi Schüpbach, Matej Krajnc (Jožef Stefan Institute), David Denberg, Tal Galili, and Yosi Keller (Bar-Ilan University) for fruitful discussions; Benny Shilo (Weizmann Institute of Science) for comments on the manuscript; Matthew Cahn (Princeton University) and the IT of Simons Foundation for technical support with computing resources; Reba Samantha and Laisa Eimont for bureaucratic assistance and Heping Jiang for stock maintenance; and lastly the Wieschaus and Shvartsman lab members for continuous support. The research was supported by the European Molecular Biology Organization long-term fellowship ALTF 215-2017 to T.S. the MCB 1516970 award from the NSF to S.Y.S. and the Howard Hughes Medical Institute to E.F.W. T.S. S.Y.S. and E.F.W. conceived and designed the project. T.S. performed algorithm development and data analysis and prepared the figures. T.S. wrote the manuscript with input from all authors. The authors declare no competing interests.
Publisher Copyright:
© 2022
PY - 2022/4/25
Y1 - 2022/4/25
N2 - Gastrulation movements in all animal embryos start with regulated deformations of patterned epithelial sheets, which are driven by cell divisions, cell shape changes, and cell intercalations. Each of these behaviors has been associated with distinct aspects of gastrulation1–4 and has been a subject of intense research using genetic, cell biological, and more recently, biophysical approaches.5–14 Most of these studies, however, focus either on cellular processes driving gastrulation or on large-scale tissue deformations.15–23 Recent advances in microscopy and image processing create a unique opportunity for integrating these complementary viewpoints.24–28 Here, we take a step toward bridging these complementary strategies and deconstruct the early stages of gastrulation in the entire Drosophila embryo. Our approach relies on an integrated computational framework for cell segmentation and tracking and on efficient algorithms for event detection. The detected events are then mapped back onto the blastoderm shell, providing an intuitive visual means to examine complex cellular activity patterns within the context of their initial anatomic domains. By analyzing these maps, we identified that the loss of nearly half of surface cells to invaginations is compensated primarily by transient mitotic rounding. In addition, by analyzing mapped cell intercalation events, we derived direct quantitative relations between intercalation frequency and the rate of axis elongation. This work is setting the stage for systems-level dissection of a pivotal step in animal development.
AB - Gastrulation movements in all animal embryos start with regulated deformations of patterned epithelial sheets, which are driven by cell divisions, cell shape changes, and cell intercalations. Each of these behaviors has been associated with distinct aspects of gastrulation1–4 and has been a subject of intense research using genetic, cell biological, and more recently, biophysical approaches.5–14 Most of these studies, however, focus either on cellular processes driving gastrulation or on large-scale tissue deformations.15–23 Recent advances in microscopy and image processing create a unique opportunity for integrating these complementary viewpoints.24–28 Here, we take a step toward bridging these complementary strategies and deconstruct the early stages of gastrulation in the entire Drosophila embryo. Our approach relies on an integrated computational framework for cell segmentation and tracking and on efficient algorithms for event detection. The detected events are then mapped back onto the blastoderm shell, providing an intuitive visual means to examine complex cellular activity patterns within the context of their initial anatomic domains. By analyzing these maps, we identified that the loss of nearly half of surface cells to invaginations is compensated primarily by transient mitotic rounding. In addition, by analyzing mapped cell intercalation events, we derived direct quantitative relations between intercalation frequency and the rate of axis elongation. This work is setting the stage for systems-level dissection of a pivotal step in animal development.
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U2 - 10.1016/j.cub.2022.02.059
DO - 10.1016/j.cub.2022.02.059
M3 - Article
C2 - 35290798
AN - SCOPUS:85129270681
SN - 0960-9822
VL - 32
SP - 1861-1868.e7
JO - Current Biology
JF - Current Biology
IS - 8
ER -