A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule

A fundamental question in biology is how morphogenesis integrates the multitude of processes that act at different scales, ranging from the molecular control of gene expression to cellular coordination in a tissue. Using machine-learning-based digital image analysis, we generated a three-dimensional...

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Main Authors: Athul Vijayan, Rachele Tofanelli, Sören Strauss, Lorenzo Cerrone, Adrian Wolny, Joanna Strohmeier, Anna Kreshuk, Fred A Hamprecht, Richard S Smith, Kay Schneitz
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/63262
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spelling doaj-0fd1977745b34159b5e061a2a61c266c2021-05-05T22:39:42ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.63262A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovuleAthul Vijayan0https://orcid.org/0000-0003-1837-6359Rachele Tofanelli1https://orcid.org/0000-0002-5196-1122Sören Strauss2Lorenzo Cerrone3Adrian Wolny4Joanna Strohmeier5Anna Kreshuk6https://orcid.org/0000-0003-1334-6388Fred A Hamprecht7Richard S Smith8https://orcid.org/0000-0001-9220-0787Kay Schneitz9https://orcid.org/0000-0001-6688-0539Plant Developmental Biology, School of Life Sciences, Technical University of Munich, Freising, GermanyPlant Developmental Biology, School of Life Sciences, Technical University of Munich, Freising, GermanyDepartment of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, GermanyHeidelberg Collaboratory for Image Processing, Dept. of Physics and Astronomy, Heidelberg University, Heidelberg, GermanyHeidelberg Collaboratory for Image Processing, Dept. of Physics and Astronomy, Heidelberg University, Heidelberg, Germany; European Molecular Biology Laboratory, Heidelberg, GermanyPlant Developmental Biology, School of Life Sciences, Technical University of Munich, Freising, GermanyEuropean Molecular Biology Laboratory, Heidelberg, GermanyHeidelberg Collaboratory for Image Processing, Dept. of Physics and Astronomy, Heidelberg University, Heidelberg, GermanyDepartment of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, GermanyPlant Developmental Biology, School of Life Sciences, Technical University of Munich, Freising, GermanyA fundamental question in biology is how morphogenesis integrates the multitude of processes that act at different scales, ranging from the molecular control of gene expression to cellular coordination in a tissue. Using machine-learning-based digital image analysis, we generated a three-dimensional atlas of ovule development in Arabidopsis thaliana, enabling the quantitative spatio-temporal analysis of cellular and gene expression patterns with cell and tissue resolution. We discovered novel morphological manifestations of ovule polarity, a new mode of cell layer formation, and previously unrecognized subepidermal cell populations that initiate ovule curvature. The data suggest an irregular cellular build-up of WUSCHEL expression in the primordium and new functions for INNER NO OUTER in restricting nucellar cell proliferation and the organization of the interior chalaza. Our work demonstrates the analytical power of a three-dimensional digital representation when studying the morphogenesis of an organ of complex architecture that eventually consists of 1900 cells.https://elifesciences.org/articles/632623D digital atlasimage analysisovulemachine learningsegmentationplants
collection DOAJ
language English
format Article
sources DOAJ
author Athul Vijayan
Rachele Tofanelli
Sören Strauss
Lorenzo Cerrone
Adrian Wolny
Joanna Strohmeier
Anna Kreshuk
Fred A Hamprecht
Richard S Smith
Kay Schneitz
spellingShingle Athul Vijayan
Rachele Tofanelli
Sören Strauss
Lorenzo Cerrone
Adrian Wolny
Joanna Strohmeier
Anna Kreshuk
Fred A Hamprecht
Richard S Smith
Kay Schneitz
A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
eLife
3D digital atlas
image analysis
ovule
machine learning
segmentation
plants
author_facet Athul Vijayan
Rachele Tofanelli
Sören Strauss
Lorenzo Cerrone
Adrian Wolny
Joanna Strohmeier
Anna Kreshuk
Fred A Hamprecht
Richard S Smith
Kay Schneitz
author_sort Athul Vijayan
title A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title_short A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title_full A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title_fullStr A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title_full_unstemmed A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title_sort digital 3d reference atlas reveals cellular growth patterns shaping the arabidopsis ovule
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-01-01
description A fundamental question in biology is how morphogenesis integrates the multitude of processes that act at different scales, ranging from the molecular control of gene expression to cellular coordination in a tissue. Using machine-learning-based digital image analysis, we generated a three-dimensional atlas of ovule development in Arabidopsis thaliana, enabling the quantitative spatio-temporal analysis of cellular and gene expression patterns with cell and tissue resolution. We discovered novel morphological manifestations of ovule polarity, a new mode of cell layer formation, and previously unrecognized subepidermal cell populations that initiate ovule curvature. The data suggest an irregular cellular build-up of WUSCHEL expression in the primordium and new functions for INNER NO OUTER in restricting nucellar cell proliferation and the organization of the interior chalaza. Our work demonstrates the analytical power of a three-dimensional digital representation when studying the morphogenesis of an organ of complex architecture that eventually consists of 1900 cells.
topic 3D digital atlas
image analysis
ovule
machine learning
segmentation
plants
url https://elifesciences.org/articles/63262
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