A Bistable Switch Mechanism for Stem Cell Domain Nucleation in the Shoot Apical Meristem.

Abstract

In plants, the stem cells residing in shoot apical meristems (SAM) give rise to above-ground tissues (Aichinger et al., 2012). Hence, the maintenance of stem cell niches is of central importance to a plant's continued growth and development (Fletcher and Meyerowitz, 2000; Gordon et al., 2009). For the flowering plant Arabidopsis thaliana, the genetic determinants of stem cell growth, division, and localization have been identified, and negative feedback between a homeodomain transcription factor, WUSCHEL (WUS), and a receptor kinase, CLAVATA (CLV), is known to play a crucial role in controlling the reservoir of stem cells in the central domain of a SAM. The morphology of plant stems and floral organs is controlled in large part by the size and stability of SAMs, which is controlled, in turn, by spatiotemporal patterns of WUS and CLV expression in meristems. For example, loss of restrictive signals in clv mutants of Arabidopsis leads to enlargement of shoot and floral meristems, resulting in extra floral organs and club-shaped siliques (Jonsson et al., 2005). The size, localization and stability of stem cell domains should be determined, in principle, by the interactions of WUS and CLV proteins, especially by their propensities to diffuse through the domain and by the rates of the molecular reactions that control their activities. Within this paradigm, reaction-diffusion (RD) models of WUS-CLV interactions have been popular mathematical models of SAM dynamics (Jonsson et al., 2005; Hohm et al., 2010; Fujita et al., 2011). In RD models, the spontaneous generation of inhomogeneous distributions of WUS and CLV in SAM domains is usually attributed to mechanisms based on a “Turing” instability (Turing, 1952; Segel and Jackson, 1972). The generic RD equations for spatiotemporal changes in the concentrations, u(x,t) and v(x,t), of two interacting proteins are ∂u∂t=f(u,v)+Du∂2u∂x2, ∂v∂t=g(u,v)+Dv∂2v∂x2, where f(u,v) and g(u,v) are nonlinear functions describing their local chemical interactions. A unique, uniform, steady-state solution, u(x,t) = u0 = constant and v(x,t) = v0, of these equations can become unstable with respect to small, non-uniform perturbations, u(x,t) = u0 + eλt·δu·cos(qx) and v(x,t) = v0 + eλt·δv·cos(qx), δu > Du, generating standing waves of wavelength l ≈ 2π/qcrit in the simulations of the RD system (Gierer and Meinhardt, 1972; Murray, 2003). At present, the diffusive lengths of CLV and WUS in SAMs have not been determined, and there is no evidence to suggest that the Turing condition (diffusivity of CLV >> diffusivity of WUS) is satisfied in the central zone of a SAM.