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

IF 3.7 2区 生物学 Q1 DEVELOPMENTAL BIOLOGY Development Pub Date : 2024-10-15 Epub Date: 2024-05-30 DOI:10.1242/dev.202590
Tejasvinee Atul Mody, Alexander Rolle, Nico Stucki, Fabian Roll, Ulrich Bauer, Kay Schneitz
{"title":"Topological analysis of 3D digital ovules identifies cellular patterns associated with ovule shape diversity.","authors":"Tejasvinee Atul Mody, Alexander Rolle, Nico Stucki, Fabian Roll, Ulrich Bauer, Kay Schneitz","doi":"10.1242/dev.202590","DOIUrl":null,"url":null,"abstract":"<p><p>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.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11168579/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Development","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1242/dev.202590","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/5/30 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"DEVELOPMENTAL BIOLOGY","Score":null,"Total":0}
引用次数: 0

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.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
三维数字胚珠拓扑分析确定了与胚珠形状多样性相关的细胞模式。
人们对组织的形态发生仍然知之甚少。在植物中,一个核心问题是发育中器官的三维细胞结构如何促成其最终形状。我们利用被子植物胚珠形状的多样性,通过对胚珠形态发生的比较分析来解决这一问题。在这里,我们提供了一个单细胞分辨率的Cardamine hirsuta胚珠发育三维数字图谱,并将其与拟南芥的等效图谱进行了比较。我们将基于神经的拓扑分析作为一种工具,用于无偏见地检测细胞结构的差异,并通过比较形态计量学和目视检查证实两个同源组织之间已识别的拓扑差异。我们发现,片状节间和球状节间的拓扑结构、细胞体积变化和组织生长模式的差异与胚珠弯曲度的差异有关。与此相反,尽管内部细胞拓扑结构和组织生长模式存在差异,但放射状、圆锥形胚珠原基和核仁却表现出相似的形状。我们的研究结果支持这样一种观点,即在三维细胞结构进化转变过程中,组织的结构组织与其对形状变化的敏感性有关。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 去求助
来源期刊
Development
Development 生物-发育生物学
CiteScore
6.70
自引率
4.30%
发文量
433
审稿时长
3 months
期刊介绍: Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.
期刊最新文献
Adhesion and shrinkage transform the rounded pupal horn into an angular adult horn in Japanese rhinoceros beetle. Dissecting the dynamic cellular transcriptional atlas of adult teleost testis development throughout the annual reproductive cycle. Interactions between U and V sex chromosomes during the life cycle of Ectocarpus. Topological analysis of 3D digital ovules identifies cellular patterns associated with ovule shape diversity. Variations in cell plasticity and proliferation underlie distinct modes of regeneration along the antero-posterior axis in the annelid Platynereis.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1