Topological analysis of 3D digital ovules identifies cellular patterns associated with ovule shape diversity.

Abstract

Tissue morphogenesis remains poorly understood. In plants, a central problem is how the 3D cellular architecture of a developing organ contributes to its final shape. We address this question through a comparative analysis of ovule morphogenesis, taking advantage of the diversity in ovule shape across angiosperms. Here, we provide a 3D digital atlas of Cardamine hirsuta ovule development at single cell resolution and compare it with an equivalent atlas of Arabidopsis thaliana. We introduce nerve-based topological analysis as a tool for unbiased detection of differences in cellular architectures and corroborate identified topological differences between two homologous tissues by comparative morphometrics and visual inspection. We find that differences in topology, cell volume variation and tissue growth patterns in the sheet-like integuments and the bulbous chalaza are associated with differences in ovule curvature. In contrast, the radialized conical ovule primordia and nucelli exhibit similar shapes, despite differences in internal cellular topology and tissue growth patterns. Our results support the notion that the structural organization of a tissue is associated with its susceptibility to shape changes during evolutionary shifts in 3D cellular architecture.

Plant phenotyping relevance

3Dデジタルアトラスと神経ベースのトポロジー解析、形態計測を用いて植物器官の細胞構造と形状を定量化しており、表現型取得・解析手法が研究の中心である。

Code and data availability

The paper's topological analysis and statistical evaluation code is publicly available on GitHub (NADO repository), with explicit availability language. The paper-specific 3D digital ovule dataset (S-BIAD957) is deposited in BioStudies, but no matching allowed URL exists for it, so it cannot be listed as an actionable,