Rocks in the auxin stream: Wound-induced auxin accumulation and ERF115 expression synergistically drive stem cell regeneration

Abstract

Plants are known for their outstanding capacity to recover from various wounds and injuries. However, it remains largely unknown how plants sense diverse forms of injury and canalize existing developmental processes into the execution of a correct regenerative response. Auxin, a cardinal plant hormone with morphogen-like properties, has been previously implicated in the recovery from diverse types of wounding and organ loss. Here, through a combination of cellular imaging and in silico modeling, we demonstrate that vascular stem cell death obstructs the polar auxin flux, much alike rocks in a stream, and causes it to accumulate in the endodermis. This in turn grants the endodermal cells the capacity to undergo periclinal cell division to repopulate the vascular stem cell pool. Replenishment of the vasculature by the endodermis depends on the transcription factor ERF115, a wound-inducible regulator of stem cell division. Although not the primary inducer, auxin is required to maintain ERF115 expression. Conversely, ERF115 sensitizes cells to auxin by activating ARF5/MONOPTEROS, an auxin-responsive transcription factor involved in the global auxin response, tissue patterning, and organ formation. Together, the wound-induced auxin accumulation and ERF115 expression grant the endodermal cells stem cell activity. Our work provides a mechanistic model for wound-induced stem cell regeneration in which ERF115 acts as a wound-inducible stem cell organizer that interprets wound-induced auxin maxima.

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

“…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.…”

“…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. However, similar to single cell death, no auxin biosynthesis could be observed during the recovery from vascular stem cell death ( Canher et al, 2020 ). However, following full root tip excision, YUCCA9-dependent auxin biosynthesis was found to be indispensable to allow regeneration of a de novo tip ( Matosevich et al, 2020 ).…”

“…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.…”

RAB GTPASE HOMOLOG 8D is required for the maintenance of both the root stem cell niche and the meristem

“…The chromate-treated med18 mutant displays a root twinning phenotype, which is associated with altered auxin response and distribution in roots (Ruiz-Aguilar et al, 2020). Furthermore, a recent study revealed that the injured provascular cells obstruct auxin flow and that this leads to auxin accumulation in endodermal cells, which triggers an auxin-dependent cell replenishment and tissue regeneration program (Canher et al, 2020). These observations suggest that auxin orchestrates post-embryonic root growth through the balance between cell death and regeneration.…”

Exchange of molecular and cellular information: a hybrid model that integrates stem cell divisions and key regulatory interactions

“…The regulatory interactions between the different cell types of the root SCN are complex and nonintuitive and computational tools are essential to understanding systemic behavior. Developmental processes such as auxin flow within the root and lateral shoot branching have been mathematically modeled to better understand and predict system-level behavior (Canher et al, 2020;Prusinkiewicz et al, 2009). Some models implement different scales of the system to simulate, understand, and predict system-level behavior as a whole.…”