Toward a 3D model of phyllotaxis based on a biochemically plausible auxin-transport mechanism

Félix Hartmann (1) , Pierre Barbier de Reuille (2) , Cris Kuhlemeier (2)

1 PIAF - Laboratoire de Physique et Physiologie Intégratives de l’Arbre en environnement Fluctuant
2 Institute of Plant Science

Polar auxin transport lies at the core of many self-organizing phenomena sustaining continuous plant organogenesis. In angiosperms, the shoot apical meristem is a potentially unique system in which the two main modes of auxin-driven patterningconvergence and canalizationco-occur in a coordinated manner and in a fully three-dimensional geometry. In the epidermal layer, convergence points form, from which auxin is canalized towards inner tissue. Each of these two patterning processes has been extensively investigated separately, but the integration of both in the shoot apical meristem remains poorly understood. We present here a first attempt of a three-dimensional model of auxin-driven patterning during phyllotaxis. We base our simulations on a biochemically plausible mechanism of auxin transport proposed by Cieslak et al. (2015) which generates both convergence and canalization patterns. We are able to reproduce most of the dynamics of PIN1 polarization in the meristem, and we explore how the epidermal and inner cell layers act in concert during phyllotaxis. In addition, we discuss the mechanism by which initiating veins connect to the already existing vascular system. Author summary The regularity of leaf arrangement around stems has long puzzled scientists. The key role played by the plant hormone auxin is now well established. On the surface of the tissue responsible for leaf formation, auxin accumulates at several points, from which new leaves eventually emerge. Auxin also guides the progression of new veins from the nascent leaves to the vascular system of the plant. Models of auxin transport have been developed to explain either auxin accumulation or auxin-driven venation. We propose the first three-dimensional model embracing both phenomena using a unifying mechanism of auxin transport. This integrative approach allows an assessment of our present knowledge on how auxin contributes to the early development of leaves. Our model reproduces many observations of auxin dynamics. It highlights how the inner and epidermal tissues act together to position new leaves. We also show that an additional, yet unknown, mechanism is required to attract new developing veins towards the main vasculature of the plant.

Mots clés: phyllotaxis; three dimensional model; polar transport; cell polarity; canalization; efflux; Biochemistry & Molecular Biology; Mathematical & Computational Biology

Mots clés: phyllotaxie; modèle 3d

Domaines: Biologie végétale

Félix Hartmann, Pierre Barbier de Reuille, Cris Kuhlemeier. Toward a 3D model of phyllotaxis based on a biochemically plausible auxin-transport mechanism. PLoS Computational Biology, 2019, 15 (4), pp.21. ⟨10.1371/journal.pcbi.1006896⟩. ⟨hal-02154563⟩