Topological analysis of multicellular complexity in the plant hypocotyl

  • Jackson M
  • Xu H
  • Duran-Nebreda S
  • et al.
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Abstract

Multicellularity arose as a result of adaptive advantages conferred to complex cellular assemblies. The arrangement of cells within organs endows higher-order functionality through a structure-function relationship, though the organizational properties of these multicellular configurations remain poorly understood. We investigated the topological properties of complex organ architecture by digitally capturing global cellular interactions in the plant embryonic stem (hypocotyl), and analyzing these using quantitative network analysis. This revealed the presence of coherent conduits of reduced path length across epidermal atrichoblast cell files. The preferential movement of small molecules along this cell type was demonstrated using fluorescence transport assays. Both robustness and plasticity in this higher order property of atrichoblast patterning was observed across diverse genetic backgrounds, and the analysis of genetic patterning mutants identified the contribution of gene activity towards their construction. This topological analysis of multicellular structural organization reveals higher order functions for patterning and principles of complex organ construction.In plants and other multicellular organisms, cells work together in tissues and organs to achieve outcomes that they would not be able to accomplish on their own. For example, the cells that make up the stem of a plant hold the leaves, flowers and other organs in place, and provide a transport network that allows molecules to move around the plant. Mapping the locations of cells within tissues and analysing the connections between them will help researchers to understand how the organisation of tissues influences the tasks cells perform.There are several different layers of tissue within a plant’s stem. The surface of the stem has a protective layer of tissue called epidermis. The epidermis contains two different types of cells known as trichoblasts and atrichoblasts, but it was not clear why these cells are organised the way they are.Arabidopsis thaliana is a small plant that is often used in studies of how plants grow and develop. Jackson et al. combined microscopy with computational techniques to study the stems of young A. thaliana seedlings. The experiments reveal that the two types of epidermal cells appear to adopt distinct roles. The trichoblasts form hair-like structures and acquire nutrients from the external environment, while their neighbours the atrichoblasts provide shortcut routes for these nutrients to be unloaded and moved up the stem. This pattern was not present in several other plant species including foxglove or poppy, suggesting it may be an adaptation in A. thaliana plants that helps them grow in the particular environments this plant faces.The findings of Jackson et al. show that cells are carefully arranged in plant stems and suggest that there is an optimal way for a plant to make a stem depending on its environment. Further work is now needed to understand how different molecules use the shortcuts provided by the atrichoblasts during plant development, and whether alternative configurations are possible. In the future, such studies may help provide a framework to genetically engineer plants that are better adapted to grow in different environments.

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Jackson, M. D., Xu, H., Duran-Nebreda, S., Stamm, P., & Bassel, G. W. (2017). Topological analysis of multicellular complexity in the plant hypocotyl. ELife, 6. https://doi.org/10.7554/elife.26023

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