A stochastic multicellular model identifies biological watermarks from disorders in self-organized patterns of phyllotaxis

Exploration of developmental mechanisms classically relies on analysis of pattern regularities. Whether disorders induced by biological noise may carry information on building principles of developmental systems is an important debated question. Here, we addressed theoretically this question using phyllotaxis, the geometric arrangement of plant aerial organs, as a model system. Phyllotaxis arises from reiterative organogenesis driven by lateral inhibitions at the shoot apex. Motivated by recurrent observations of disorders in phyllotaxis patterns, we revisited in depth the classical deterministic view of phyllotaxis. We developed a stochastic model of primordia initiation at the shoot apex, integrating locality and stochasticity in the patterning system. This stochastic model recapitulates phyllotactic patterns, both regular and irregular, and makes quantitative predictions on the nature of disorders arising from noise. We further show that disorders in phyllotaxis instruct us on the parameters governing phyllotaxis dynamics, thus that disorders can reveal biological watermarks of developmental systems. DOI: http://dx.doi.org/10.7554/eLife.14093.001
eLife digest Plants grow throughout their lifetime, forming new flowers and leaves at the tips of their stems through a patterning process called phyllotaxis, which occurs in spirals for a vast number of plant species. The classical view suggests that the positioning of each new leaf or flower bud at the tip of a growing stem is based on a small set of principles. This includes the idea that buds produce inhibitory signals that prevent other buds from forming too close to each other. When computational models of phyllotaxis follow these ‘deterministic’ principles, they are able to recreate the spiral pattern the buds form on a growing stem. In real plants, however, the spiral pattern is not always perfect. The observed disturbances in the pattern are believed to reflect the presence of random fluctuations – regarded as noise – in phyllotaxis. Here, using numerical simulations, Refahi et al. noticed that the patterns of inhibitory signals in a shoot tip pre-determine the locations of several competing sites where buds could form in a robust manner. However, random fluctuations in the way cells perceive these inhibitory signals could greatly disturb the timing of organ formation and affect phyllotaxis patterns. Building on this, Refahi et al. created a new computational model of bud patterning that takes into account some randomness in how cells perceive the inhibitory signals released by existing buds. The model can accurately recreate the classical spiral patterns of buds and also produces occasional disrupted patterns that are similar to those seen in real plants. Unexpectedly, Refahi et al. show that these ‘errors’ reveal key information about how the signals that control phyllotaxis might work. These findings open up new avenues of research into the role of noise in phyllotaxis. The model can be used to predict how altering the activities of genes or varying plant growth conditions might disturb this patterning process. Furthermore, the work highlights how the structure of disturbances in a biological system can shed new light on how the system works. DOI: http://dx.doi.org/10.7554/eLife.14093.002