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

Abstract

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

Fibonacci spirals in a brown alga [Sargassum muticum (Yendo) Fensholt] and in a land plant [Arabidopsis thaliana (L.) Heynh.]: a case of morphogenetic convergence

“…As was demonstrated by simulations [15] and by measurements performed on the stem of sunflowers [17], permutations in the order of formation of the primordia can then become frequent. The effect of a natural noise on phyllotaxis has been investigated recently by Mirabet et al [32] and Refahi et al [33] and was shown to generate such permutations, in excellent agreement with the botanical data. These permutations have little effect on the parastichy order but the plastochrone values as well as the sequence of angles are both strongly disturbed.…”

“…However, the scatter in the values of <φ PM > and <φ M > has a more fundamental origin [15,17,32,33]. The phyllotactic patterns are generated sequentially by the formation of successive primordia.…”

Stochastic occurrence of trimery from pentamery in floral phyllotaxis of Anemone (Ranunculaceae)

“…As energy decreases, the chance of a new primordium emerging increases. For example, Arabidopsis inflorescence phyllotaxis has several local energy minima, in addition to the global minimum at divergence angle φ, which is considered to be the cause of stochasticity in angular organs positions [17,18]. For simplicity, we assume that the five organs are already arranged in a whorl with equal divergence angle φ (Eq.…”

Auxin 2016: a burst of auxin in the warm south of China

“…The timing of lateral organ initiation at the shoot apical meristem is established by auxin-based inhibitory fields, and Teva Vernoux (École normale supérieure de Lyon, Lyon, France) showed that this timing is noisy, inducing defects in shoot phyllotaxis (Besnard et al, 2014). He further demonstrated that including stochasticity in signal perception in an inhibitory-field model can recapitulate these biological observations, suggesting that making a new organ in response to auxin and other signals could be based on a probabilistic decision (Refahi et al, 2016). Riccardo di Mambro from Sabrina Sabatini's laboratory (La Sapienza University, Rome, Italy) showed how they used a cellbased auxin transport model to analyze the interaction between auxin and cytokinins in setting root meristem size.…”