Abstract

The patterning of the Arabidopsis root epidermis depends on a genetic regulatory network that operates both within and between cells. Genetic studies have identified a number of key components of this network, but a clear picture of the functional logic of the network is lacking. Here, we integrate existing genetic and biochemical data in a mathematical model that allows us to explore both the sufficiency of known network interactions and the extent to which additional assumptions about the model can account for wild-type and mutant data. Our model shows that an existing hypothesis concerning the autoregulation of WEREWOLF does not account fully for the expression patterns of components of the network. We confirm the lack of WEREWOLF autoregulation experimentally in transgenic plants. Rather, our modelling suggests that patterning depends on the movement of the CAPRICE and GLABRA3 transcriptional regulators between epidermal cells. Our combined modelling and experimental studies show that WEREWOLF autoregulation does not contribute to the initial patterning of epidermal cell fates in the Arabidopsis seedling root. In contrast to a patterning mechanism relying on local activation, we propose a mechanism based on lateral inhibition with feedback. The active intercellular movements of proteins that are central to our model underlie a mechanism for pattern formation in planar groups of cells that is centred on the mutual support of two cell fates rather than on local activation and lateral inhibition.

Highlights

  • The cells of the Arabidopsis root epidermis emerge from the initial cells in the root meristem with the potential to adopt either of two cell fates—trichoblasts or atrichoblasts

  • At the core of this network lie protein complexes centred on the basic helix-loop-helix proteins GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) and the WD40-repeat– containing protein TRANSPARENT TESTA GLABRA (TTG)

  • We show by a combination of mathematical modelling and experimental studies that WER autoregulation does not play a significant role in the epidermal patterning network, and propose a mechanism for patterning that depends on the mutual support of the two epidermal cell fates

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Summary

Introduction

The cells of the Arabidopsis root epidermis emerge from the initial cells in the root meristem with the potential to adopt either of two cell fates—trichoblasts (cells that can go on to differentiate as root hair cells) or atrichoblasts (that differentiate into non–hair-bearing epidermal cells). The two cell types are arranged in a stereotyped spatial pattern, with files of trichoblasts overlying two cortical cells (the H position) separated by files of atrichoblasts in contact with only one underlying cortical cell (the N position) (Figure 1) [1,2] This fixed pattern does not result from lineage restriction, but depends on a combination of positional information from the cortex and the operation of a genetic regulatory network within the epidermis [3,4,5]. At the core of this network lie protein complexes centred on the basic helix-loop-helix proteins GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) and the WD40-repeat– containing protein TRANSPARENT TESTA GLABRA (TTG).

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