A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves

Abstract

Trichome patterning in Arabidopsis serves as a model system for de novo pattern formation in plants.It is thought to typify the theoretical activator-inhibitor mechanism, although this hypothesis has never been challenged by a combined experimental and theoretical approach. By integrating the key genetic and molecular data of the trichome patterning system, we developed a new theoretical model that allows the direct testing of the effect of experimental interventions and in the prediction of patterning phenotypes. We show experimentally that the trichome inhibitor TRIPTYCHON is transcriptionally activated by the known positive regulators GLABRA1 and GLABRA3. Further, we demonstrate by particle bombardment of protein fusions with GFP that TRIPTYCHON and CAPRICE but not GLABRA1 and GLABRA3 can move between cells. Finally, theoretical considerations suggest promoter swapping and basal overexpression experiments by means of which we are able to discriminate three biologically meaningful variants of the trichome patterning model. Our study demonstrates that the mutual interplay between theory and experiment can reveal a new level of understanding of how biochemical mechanisms can drive biological patterning processes.

Temporal Control of Trichome Distribution by MicroRNA156-TargetedSPLGenes inArabidopsis thaliana

“…Nevertheless, the results presented here do not exclude the possibility that other flowering factors also participate in controlling trichome formation in specific floral organs. In the lateral inhibition model proposed for rosette leaf trichome pattering, the negative regulator genes, such as TRY, are activated in trichome cells by the GL1-GL3-TTG1 protein complex and moved to neighboring cells to repress trichome initiation (Schellmann et al, 2002;Digiuni et al, 2008). Consistent with GL1, the TRY expression in rosette leaves is also trichome specific (Schellmann et al, 2002;Esch et al, 2003).…”

“…The singlerepeat MYB proteins can move from the trichome into neighboring cells where they compete with GL1 for the binding site of GL3 to prevent the formation of the active protein complex, resulting in blockage of trichome initiation. This lateral inhibition mechanism explains how the trichome spacing pattern is generated in rosette leaves (Schellmann et al, 2002;Digiuni et al, 2008).…”

The Chemical Kinetics of Shape Determination in Plants

“…B) SEM of trichomes (protective hairs) on the underside of a leaf of Arabidopsis; image from Deeks et al (2007), with permission. Digiuni et al (2008) found that trichomes are patterned by an RD mechanism, by quantitatively matching experimental manipulations of specific trichome genes with a dynamic (RD) model of trichome gene interactions.…”

“…Several groups have recently published work on RD mechanisms in specific genetic pathways in Arabidopsis development, identifying specific known molecules as Turing morphogens. Digiuni et al (2008) determined that trichomes, protective hairs on the undersides of Arabidopsis leaves (Fig. 9B), are patterned by an RD mechanism.…”

9.1 Modeling the Positioning of Trichomes on the Leaves of Plants

“…Various models have been proposed including (a) activator-inhibitor reaction-diffusion (AIRD) PDEs models [13], (b) cellular signaling and switching models [7,25], (c) phenomenological genetic models-logical descriptions of the gene activity in terms of diagrammatic models, and (d) systems of ordinary differential equations which model the known genetics and a biological interpretation of the roles of the genes [6].…”