Topological analysis of multicellular complexity in the plant hypocotyl

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.