von Wangenheim, DanielISTA ; Fangerau, Jens; Schmitz, Alexander; Smith, Richard S; Leitte, Heike; Stelzer, Ernst H; Maizel, Alexis
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.
We thank M.J. Bennett, L. Laplaze, and S. Lemke for their helpful comments. This work was supported by the Land Baden-Württemberg, the Chica und Heinz Schaller Stiftung, the CellNetworks cluster of excellence, and the Boehringer Ingelheim Fond (to J.F. and A.M.) and the Cluster of Excellence “Macromolecular Complexes” at the Goethe University Frankfurt am Main (CEF-MC II; DFG Project EXC 115; to D.v.W., A.S., and E.H.K.S.).
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von Wangenheim D, Fangerau J, Schmitz A, et al. Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Current Biology. 2016;26(4):439-449. doi:10.1016/j.cub.2015.12.047
von Wangenheim, D., Fangerau, J., Schmitz, A., Smith, R., Leitte, H., Stelzer, E., & Maizel, A. (2016). Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Current Biology. Cell Press. https://doi.org/10.1016/j.cub.2015.12.047
Wangenheim, Daniel von, Jens Fangerau, Alexander Schmitz, Richard Smith, Heike Leitte, Ernst Stelzer, and Alexis Maizel. “Rules and Self-Organizing Properties of Post-Embryonic Plant Organ Cell Division Patterns.” Current Biology. Cell Press, 2016. https://doi.org/10.1016/j.cub.2015.12.047.
D. von Wangenheim et al., “Rules and self-organizing properties of post-embryonic plant organ cell division patterns,” Current Biology, vol. 26, no. 4. Cell Press, pp. 439–449, 2016.
von Wangenheim D, Fangerau J, Schmitz A, Smith R, Leitte H, Stelzer E, Maizel A. 2016. Rules and self-organizing properties of post-embryonic plant organ cell division patterns. Current Biology. 26(4), 439–449.
von Wangenheim, Daniel, et al. “Rules and Self-Organizing Properties of Post-Embryonic Plant Organ Cell Division Patterns.” Current Biology, vol. 26, no. 4, Cell Press, 2016, pp. 439–49, doi:10.1016/j.cub.2015.12.047.