Nucleation of stem cell domains in a bistable activator-inhibitor model of the shoot apical meristem

Shoot apical meristems (SAMs) give rise to all above-ground tissues of a plant. Expansion of meristematic tissue is derived from the growth and division of stem cells that reside in a central zone of the SAM. This reservoir of stem cells is maintained by expression of a transcription factor WUSCHEL that is responsible for the development of stem cells in the central zone. WUSCHEL expression is self-activating and downregulated by a signaling pathway initiated by CLAVATA proteins, which are upregulated by WUSCHEL. This classic activator-inhibitor network can generate localized patterns of WUSCHEL activity by a Turing instability provided certain constraints on reaction rates and diffusion constants of WUSCHEL and CLAVATA are satisfied, and most existing mathematical models of nucleation and confinement of stem cells in the SAM rely on Turing's mechanism. However, Turing patterns have certain properties that are inconsistent with observed patterns of stem cell differentiation in the SAM. As an alternative mechanism, we propose a model for stem cell confinement based on a bistable-switch in WUSCHEL-CLAVATA interactions. We study the bistable-switch mechanism for pattern formation in a spatially continuous domain and in a discrete cellularized tissue in the presence of a non-uniform field of a rapidly diffusing hormone. By comparing domain formation by Turing and bistable-switch mechanisms in these contexts, we show that bistable switching provides a superior account of nucleation and confinement of the stem cell domain under reasonable assumptions on reaction rates and diffusion constants. Published under an exclusive license by AIP Publishing.

Automated summary

Shoot apical meristems (SAMs) are responsible for the development of above-ground tissues in plants. The growth and expansion of SAMs rely on the division of stem cells in a central zone, which is regulated by a transcription factor called WUSCHEL. WUSCHEL is self-activating and downregulated by a signaling pathway involving CLAVATA proteins. While most mathematical models of stem cell confinement in the SAM rely on Turing's mechanism, this study proposes a bistable-switch model based on interactions between WUSCHEL and CLAVATA. Comparisons between the two mechanisms demonstrate that the bistable-switch provides a better explanation for the nucleation and confinement of stem cells.