Abstract
Rho GTPases play crucial roles in cell polarity and pattern formation. ROPs, Rho of plant GTPases, are widely involved in cell wall patterning in plants, yet the molecular mechanism underlying their action remains unknown. Arabidopsis ROP11 is locally activated to form plasma membrane domains, which direct formation of cell wall pits in metaxylem vessel cells through interaction with cortical microtubules. Here, we show that the pattern formation of cell wall pits is governed by ROP activation via a reaction-diffusion mechanism. Genetic analysis and reconstructive assays revealed that ROPGEF4/7 and ROPGAP3/4, which encode ROP activators and inactivators, respectively, regulated the formation of ROP-activated domains; these in turn determined the pattern of cell wall pits. Mathematical modelling showed that ROP-activation cycle generated ROP domains by reaction-diffusion mechanism. The model predicted that a positive feedback and slow diffusion of ROP11-ROPGEF4 complex were required to generate ROP-activated domains. ROPGEF4 formed a dimer that interacted with activated ROP11 in vivo, which could provide positive feedback for ROP activation. ROPGEF4 was highly stable on the plasma membrane and inhibited ROP11 diffusion. Our study indicated that ROP-based reaction-diffusion system self-organizes ROP-activated domains, thereby determines the pit pattern of metaxylem vessels.
Highlights
Pattern formation during plant and animal development is a fundamental issue in biology
We found that ROPGEF4 formed a dimer that interacted in vivo with activated ROP11, which could provide positive feedback for ROP activation
In Arabidopsis metaxylem vessels, ROPGEF4, which encodes a plant-specific guanine nucleotide exchanging factors (GEFs) family protein, is partially required for secondary cell wall pit formation[17], suggesting that other ROPGEF genes function in metaxylem vessels
Summary
Pattern formation during plant and animal development is a fundamental issue in biology. Rho/Rac GTPases are conserved signalling enzymes that play central roles in directing subcellular patterns[9,10,11,12,13] They are present in two states: a GTP-bound active form and a GDP-bound inactive form. We recently reported that cortical microtubules regulate the shape of ROP-activated plasma membrane domains through IQD13 and CORD1, which confines and releases ROP-activated domains, respectively[18,19] As it is still unclear how ROP-activated domains are generated and what determines the pattern of ROP-activated domains, we investigated the mechanism underlying secondary cell wall pit patterning using genetics, reconstructive techniques, and mathematical modelling. Our study indicated that ROP-activation/inactivation cycle self-organizes ROP-activated domains via a reaction-diffusion mechanism, thereby determines the pit pattern in secondary cell walls
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