Root growth responses to mechanical impedance are regulated by a network of ROS, ethylene and auxin signalling in Arabidopsis.

Amy G R Jacobsen,Keith Lindsey,George Jervis,Jennifer F Topping,Jian Xu

doi:10.1111/nph.17180

Abstract

Summary The growth and development of root systems is influenced by mechanical properties of the substrate in which the plants grow. Mechanical impedance, such as by compacted soil, can reduce root elongation and limit crop productivity.To understand better the mechanisms involved in plant root responses to mechanical impedance stress, we investigated changes in the root transcriptome and hormone signalling responses of Arabidopsis to artificial root barrier systems in vitro.We demonstrate that upon encountering a barrier, reduced Arabidopsis root growth and a characteristic ‘step‐like’ growth pattern is due to a reduction in cell elongation associated with changes in signalling gene expression. Data from RNA‐sequencing combined with reporter line and mutant studies identified essential roles for reactive oxygen species, ethylene and auxin signalling during the barrier response.We propose a model in which early responses to mechanical impedance include reactive oxygen signalling integrated with ethylene and auxin responses to mediate root growth changes. Inhibition of ethylene responses allows improved growth in response to root impedance, an observation that may inform future crop breeding programmes.

Highlights

When growing through soils, plant roots must be able to respond to a range of environmental cues and rely on flexible growth to adapt to changing conditions
We demonstrate that the early response involves a transcriptional activation of genes encoding components of reactive oxygen species (ROS) signalling associated with ethylene and auxin signalling, and show that each is required for the impedance response
Consistent with previous studies (Massa & Gilroy, 2003; Lee et al, 2020), roots were found to attempt to rapidly bend away from obstacles, forming a ‘step-like’ growth pattern where the root grows parallel to the obstacle while the root tip maintains contact with the barrier

Summary

Introduction

Plant roots must be able to respond to a range of environmental cues and rely on flexible growth to adapt to changing conditions. Various stress conditions in soils limit root elongation, including insufficient nutrients, oxygen or water, and physical barriers (Bengough et al, 2006). As plant roots navigate the soil environment, they encounter physical barriers and must be able to adapt their growth in order to respond to mechanical impedance. Penetrometer resistance is commonly used as a measure of soil strength, and increased resistance correlates with reduced root elongation (Whitmore & Whalley, 2009; Bengough et al, 2011)

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Conclusion