Mathematical modeling of plant cell fate transitions controlled by hormonal signals

Abstract

Coordination of fate transition and cell division is crucial to maintain the plant architecture and to achieve efficient production of plant organs. In this paper, we analysed the stem cell dynamics at the shoot apical meristem (SAM) that is one of the plant stem cells locations. We designed a mathematical model to elucidate the impact of hormonal signaling on the fate transition rates between different zones corresponding to slowly dividing stem cells and fast dividing transit amplifying cells. The model is based on a simplified two-dimensional disc geometry of the SAM and accounts for a continuous displacement towards the periphery of cells produced in the central zone. Coupling growth and hormonal signaling results in a nonlinear system of reaction-diffusion equations on a growing domain with the growth velocity depending on the model components. The model is tested by simulating perturbations in the level of key transcription factors that maintain SAM homeostasis. The model provides new insights on how the transcription factor HECATE is integrated in the regulatory network that governs stem cell differentiation. 1 SummaryPlants continuously generate new organs such as leaves, roots and flowers. This process is driven by stem cells which are located in specialized regions, so-called meristems. Dividing stem cells give rise to offspring that, during a process referred to as cell fate transition, become more specialized and give rise to organs. Plant architecture and crop yield crucially depend on the regulation of meristem dynamics. To better understand this regulation, we develop a computational model of the shoot meristem. The model describes the meristem as a two-dimensional disk that can grow and shrink over time, depending on the concentrations of the signalling factors in its interior. This allows studying how the non-linear interaction of multiple transcription factors is linked to cell division and fate-transition. We test the model by simulating perturbations of meristem signals and comparing them to experimental data. The model allows simulating different hypotheses about signal effects. Based on the model we study the specific role of the transcription factor HECATE and provide new insights in its action on cell dynamics and in its interrelation with other known transcription factors in the meristem. 4 ing molecules. Such models have been applied e.g., to investigate cytokinin signaling [11] and patterning of the shoot apical meristem [14,17]. To investigate the impact of HEC on fate transition and proliferation rates of cells in the CZ and PZ, we have recently proposed a model based on the population dynamics approach, in which dynamics of different cell subpopulations are described by ordinary differential equations [9]. Such approach allows tracking how changes in cell proliferation, fate transition, primordia formation and primordia separation affect the time evolution and steady-state size of the different SAM zones but does not take into account spatio-temporal dynamics of the underlying signal...

A mathematical model for understanding synergistic regulations and paradoxical feedbacks in the shoot apical meristem

“…In particular, we considered signals that regulate WUS expression from both the middle SAM and peripheral regions. This differs from previous models which focused on the middle SAM region around the apical-basal axis [11] , [13] , [16] , [17] , [18] , [22] , [23] , [24] , [25] . Our model shows how the system combines the peripheral signal EPFL with the CLV3 signal originating from the top central SAM to restrict WUS expression to the organizing center in the meristem rib.…”

“…Previous mathematical models of SAM patterning have been focused on the negative feedback between WUS and CLV3, as well as other factors controlling their expressions along the apical-basal axis [11] , [13] , [16] , [17] , [18] , [19] , [20] , [22] , [23] , [24] , [25] . Here, we built a two-dimensional model incorporating elements of these previous models with the potent lateral regulator EPFL that was recently characterized ( Fig.…”

“…More recent discoveries show that the separation of WUS and CLV3 expressing regions is driven by additional signals originating from the basal zones of the SAM, such as high concentrations of WUS and/or HAIRY MERISTEM (HAM) [13] , [14] , [15] , and these signals prevent CLV3 expression below the subepidermal layer. Mathematical models have been used in numerous studies to describe the dynamics of gene activities in the SAM quantitatively, and have improved our understanding of the complex molecular and cellular networks controlling SAM patterning [11] , [13] , [16] , [17] , [18] , [19] , [20] , [21] , [22] , [23] , [24] , [25] . These models have revealed the key role of negative feedback in maintaining homeostasis, as well as the mechanisms underlying the separation between CLV3 and WUS expressing domains.…”

Cytokinin Signaling and De Novo Shoot Organogenesis

“…The central zone includes three separate cell layers that form the epidermis (L1), ground tissue (L2) and vasculature (L3). The induction and maintenance of the stem cell fate are conditioned by the activity of the organizing center (OC), which is situated directly underneath the SC area [42,43]. The transcriptional activation of WUSCHEL (WUS) is considered to be a critical molecular event triggering CK-induced shoot organogenesis.…”

“…In the process of SAM establishment, WUS is thought to define the organizing center. Therefore, WUS expression is substantial for the de novo organization of the shoot stem cell niches that generate signals that control the balance between self-renewal processes and the production of daughter cells that can differentiate into new tissues [43], and induction of stem cell fate in the pool of cells that overlie the OC. Meristem maintenance depends upon a balance between stem cell division within the meristem center and differentiation toward the periphery.…”