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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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Autores principales: Vijayan, Athul, Tofanelli, Rachele, Strauss, Sören, Cerrone, Lorenzo, Wolny, Adrian, Strohmeier, Joanna, Kreshuk, Anna, Hamprecht, Fred A, Smith, Richard S, Schneitz, Kay
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7787667/
https://www.ncbi.nlm.nih.gov/pubmed/33404501
http://dx.doi.org/10.7554/eLife.63262
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author Vijayan, Athul
Tofanelli, Rachele
Strauss, Sören
Cerrone, Lorenzo
Wolny, Adrian
Strohmeier, Joanna
Kreshuk, Anna
Hamprecht, Fred A
Smith, Richard S
Schneitz, Kay
author_facet Vijayan, Athul
Tofanelli, Rachele
Strauss, Sören
Cerrone, Lorenzo
Wolny, Adrian
Strohmeier, Joanna
Kreshuk, Anna
Hamprecht, Fred A
Smith, Richard S
Schneitz, Kay
author_sort Vijayan, Athul
collection PubMed
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.
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spelling pubmed-77876672021-01-11 A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule Vijayan, Athul Tofanelli, Rachele Strauss, Sören Cerrone, Lorenzo Wolny, Adrian Strohmeier, Joanna Kreshuk, Anna Hamprecht, Fred A Smith, Richard S Schneitz, Kay eLife Developmental Biology 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. eLife Sciences Publications, Ltd 2021-01-06 /pmc/articles/PMC7787667/ /pubmed/33404501 http://dx.doi.org/10.7554/eLife.63262 Text en © 2021, Vijayan et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Developmental Biology
Vijayan, Athul
Tofanelli, Rachele
Strauss, Sören
Cerrone, Lorenzo
Wolny, Adrian
Strohmeier, Joanna
Kreshuk, Anna
Hamprecht, Fred A
Smith, Richard S
Schneitz, Kay
A digital 3D reference atlas reveals cellular growth patterns shaping the Arabidopsis ovule
title 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_short 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
topic Developmental Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7787667/
https://www.ncbi.nlm.nih.gov/pubmed/33404501
http://dx.doi.org/10.7554/eLife.63262
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