Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots

Abstract

<jats:p>Wound healing in plant tissues, consisting of rigid cell wall-encapsulated cells, represents a considerable challenge and occurs through largely unknown mechanisms distinct from those in animals. Owing to their inability to migrate, plant cells rely on targeted cell division and expansion to regenerate wounds. Strict coordination of these wound-induced responses is essential to ensure efficient, spatially restricted wound healing. Single-cell tracking by live imaging allowed us to gain mechanistic insight into the wound perception and coordination of wound responses after laser-based wounding in<jats:italic>Arabidopsis</jats:italic>root. We revealed a crucial contribution of the collapse of damaged cells in wound perception and detected an auxin increase specific to cells immediately adjacent to the wound. This localized auxin increase balances wound-induced cell expansion and restorative division rates in a dose-dependent manner, leading to tumorous overproliferation when the canonical TIR1 auxin signaling is disrupted. Auxin and wound-induced turgor pressure changes together also spatially define the activation of key components of regeneration, such as the transcription regulator ERF115. Our observations suggest that the wound signaling involves the sensing of collapse of damaged cells and a local auxin signaling activation to coordinate the downstream transcriptional responses in the immediate wound vicinity.</jats:p>

Breaking Bad News: Dynamic Molecular Mechanisms of Wound Response in Plants

“…DAMPs released from wounds signal the surrounding intact cells via Ca 2+ , ROS, phosphorylation, and electrical signaling to mount defense gene expression. Most likely, direct physical responses, such as changes in mechanical forces and cell pressure surrounding the wound, play a pronounced signaling role, although these are largely unknown ( Routier-Kierzkowska et al, 2012 ; Hoermayer et al, 2020 ). In parallel and depending on the severity of damage, systemic signals are propagated from the wound site to the rest of the plant, comprising leaf-to-leaf, root-to-root, leaf-to-root, and root-to-leaf signaling.…”

“…Auxin accumulates within a day at the wound site and directly activates expression of the WUSCHEL related homeobox 11 ( WOX11 ) transcription factor, which works redundantly with WOX12 to enable the transition of the local cambium cells to root founder cells within 4 days following the cut ( Liu et al, 2014 ; Hu and Xu, 2016 ). Accumulating evidence from recent publications on root regeneration emphasizes the importance of auxin during the replenishment of a single cell, a cluster of damaged root cells, or even regeneration of a complete de novo root tip ( Canher et al, 2020 ; Hoermayer et al, 2020 ; Matosevich et al, 2020 ). Depending on the severity and type of damage, the mode of action that allows for sufficient auxin accumulation in order to facilitate the regeneration process varies.…”

“…Depending on the severity and type of damage, the mode of action that allows for sufficient auxin accumulation in order to facilitate the regeneration process varies. Upon death of a single cell, for example, following laser ablation, a strictly localized auxin signaling, independent of biosynthesis or active transport, coordinates the wounding response ( Hoermayer et al, 2020 ). Upon death of a group of vascular stem cells, for example, by bleomycin-induced DNA damage, the natural auxin flow is disrupted through downregulation of auxin transporters, resulting in an auxin redistribution, much alike rocks in a stream.…”

“…Being the death of a single cell, stem cell damage or even removal of the entire root tip, ERF115 expression is instantly activated within 1–2 h in the adjacent cells and plays a key role in stimulating these cells to activate the cell division program ( Heyman et al, 2016 ; Zhang et al, 2016 ). Although not being the initial trigger, auxin is required to maintain ERF115 expression following tissue damage ( Canher et al, 2020 ; Hoermayer et al, 2020 ), leaving the question open about the initial trigger activating this key regeneration granting factor following wounding.…”

Regulation of touch dependantde novoroot regeneration in Arabidopsis

“…Recently, it was shown that regeneration of specific cell types in root was influenced by osmotic pressure, suggesting that mechanical signalling pathways can be instrumental in regeneration(Hoermayer et al , 2020). Therefore, it is possible that mechanical signals can instruct DNRR.…”