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.