RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis.

Beata Orman-Ligeza,Claire Périlleux,Tom Beeckman,Boris Parizot,Malcolm J Bennett,Xavier Draye,Frank Van Breusegem,Ana Fernandez,Riet De Rycke,Ellie Himschoot

doi:10.1242/dev.136465

Abstract

Lateral root (LR) emergence represents a highly coordinated process in which the plant hormone auxin plays a central role. Reactive oxygen species (ROS) have been proposed to function as important signals during auxin-regulated LR formation; however, their mode of action is poorly understood. Here, we report that Arabidopsis roots exposed to ROS show increased LR numbers due to the activation of LR pre-branch sites and LR primordia (LRP). Strikingly, ROS treatment can also restore LR formation in pCASP1:shy2-2 and aux1 lax3 mutant lines in which auxin-mediated cell wall accommodation and remodeling in cells overlying the sites of LR formation is disrupted. Specifically, ROS are deposited in the apoplast of these cells during LR emergence, following a spatiotemporal pattern that overlaps the combined expression domains of extracellular ROS donors of the RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH). We also show that disrupting (or enhancing) expression of RBOH in LRP and/or overlying root tissues decelerates (or accelerates) the development and emergence of LRs. We conclude that RBOH-mediated ROS production facilitates LR outgrowth by promoting cell wall remodeling of overlying parental tissues.

Highlights

Root branching plays a crucial role enhancing the ability of the root system to explore and take up water and nutrients from the soil environment
An interplay between auxin and Reactive oxygen species (ROS) signaling during Lateral root (LR) formation We initially analyzed datasets from published microarray experiments (Affymetrix ATH1 arrays) that relate to auxinmediated LR formation or ROS responses
In the LR inducible system (LRIS) system, seedlings are grown for 3 days on the auxin transport inhibitor 1-N-naphthylphthalamic acid (NPA) and treated for 2 h with synthetic auxin-related signaling molecules 1-naphthaleneacetic acid (NAA) or naxillin to trigger synchronous LR formation in root pericycle cells (De Rybel et al, 2012; Vanneste et al, 2005)

Summary

Introduction

Root branching plays a crucial role enhancing the ability of the root system to explore and take up water and nutrients from the soil environment. The SHY2 signaling module triggers changes in cell volume and wall properties termed ‘spatial accommodation’, thereby facilitating the passage of LRP (Vermeer et al, 2014). In the cortex and the epidermal cells overlying the expanding LRP, cell wall remodeling enzymes are induced to facilitate LRP emergence (GonzalezCarranza et al, 2007; Lewis et al, 2013; Neuteboom et al, 1999; Swarup et al, 2008). The activity of the auxin influx carrier LIKE AUX1 3 (LAX3) localizes the auxin-induced expression of these cell wall remodeling genes that degrade the pectin-rich middle lamellae. LRP emergence through the cortex and epidermis is hampered in lax mutants (Swarup et al, 2008) and defects in genes involved in cell wall formation increase the rate of LRP emergence, as shown recently with mutants with impaired cell wall biosynthesis (Roycewicz and Malamy, 2014) and abscission (Kumpf et al, 2013)

Methods

Results

Conclusion