Rules and Self-Organizing Properties of Post-embryonic Plant Organ Cell Division Patterns

Plants form new organs with patterned tissue organization throughout their lifespan. It is unknown whether this robust post-embryonic organ formation results from stereotypic dynamic processes, in which the arrangement of cells follows rigid rules. Here, we combine modeling with empirical observations of whole-organ development to identify the principles governing lateral root formation in Arabidopsis. Lateral roots derive from a small pool of founder cells in which some take a dominant role as seen by lineage tracing. The first division of the founders is asymmetric, tightly regulated, and determines the formation of a layered structure. Whereas the pattern of subsequent cell divisions is not stereotypic between different samples, it is characterized by a regular switch in division plane orientation. This switch is also necessary for the appearance of patterned layers as a result of the apical growth of the primordium. Our data suggest that lateral root morphogenesis is based on a limited set of rules. They determine cell growth and division orientation. The organ-level coupling of the cell behavior ensures the emergence of the lateral root’s characteristic features. We propose that self-organizing, non-deterministic modes of development account for the robustness of plant organ morphogenesis. [Display omitted] •The first full four-dimensional atlas of lateral root formation is provided•The timing of emergence of layers is stereotypic relative to the number of cells•The contribution of each founder cell to the primordium is not stereotypical•The initial asymmetric division has long-term effects on division patterns von Wangenheim et al. use modeling and light sheet microscopy observations for an in-depth analysis of cell division patterns during lateral root formation in Arabidopsis. The orthogonal shifts in division planes and the layered organization of the root can be explained by simple rules that lead to global self-organizing patterns.