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

Abstract

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.

Between Stress and Response: Function and Localization of Mechanosensitive Ca2+ Channels in Herbaceous and Perennial Plants

“…The typical responses of roots encountering an obstacle are a reduction of root growth and a resulting "step-like" growth pattern, with only the root tip remaining in contact with the barrier surface. By RNA-seq approaches performed on whole roots of Arabidopsis seedlings collected either 6 or 30 h after barrier contact, combined with reporter line and mutant studies, Jacobsen et al [130] showed significant changes in reactive oxygen species (ROS), ethylene and auxin signaling pathways, confirming several previous studies. In particular, they demonstrated that when ethylene signaling is perturbed in ethylene-insensitive mutants, the root growth is less inhibited than in WT after barrier contact.…”

Ethylene Signaling Facilitates Plant Adaption to Physical Barriers

“…Thus, the roots need to continuously adjust their morphological structures to respond to ever-changing local soil environments. The physically impeded roots display diverse morphological alterations, such as inhibition of root elongation and increase of radial dimension, resembling the morphological changes observed when roots are grown in the presence of ethylene ( Jacobsen et al, 2021 ). Consistent with these observations, when ethylene biosynthesis or signaling is repressed, the degree of root response to mechanical impedance is significantly alleviated ( Santisree et al, 2011 ).…”

To Fight or to Grow: The Balancing Role of Ethylene in Plant Abiotic Stress Responses

“…Similarly, ethylene signaling and ethylene-triggered downstream auxin and ROS signaling act together in the inhibition of root hair growth caused by boron deficiency, as evidenced by genetic and chemical treatment analyses [ 156 , 157 ]. Moreover, auxin, ethylene, and ROS also cooperate in regulating root architecture in response to mechanical impedance stress [ 158 ].…”