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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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 |
work_keys_str_mv |
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