The wound-activated ERF15 transcription factor drives Marchantia polymorpha regeneration by activating an oxylipin biosynthesis feedback loop

Abstract

The regenerative potential in response to wounding varies widely among species. Within the plant lineage, the liverwort Marchantia polymorpha displays an extraordinary regeneration capacity. However, its molecular pathways controlling the initial regeneration response are unknown. Here, we demonstrate that the Mp ERF15 transcription factor gene is instantly activated after wounding and is essential for gemmaling regeneration following tissue incision. MpERF15 operates both upstream and downstream of the MpCOI1 oxylipin receptor by controlling the expression of oxylipin biosynthesis genes. The resulting rise in the oxylipin dinor-12-oxo-phytodienoic acid (dn-OPDA) levels results in an increase in gemma cell number and apical notch organogenesis, generating highly disorganized and compact thalli. Our data pinpoint Mp ERF15 as a key factor activating an oxylipin biosynthesis amplification loop after wounding, which eventually results in reactivation of cell division and regeneration. We suggest that the genetic networks controlling oxylipin biosynthesis in response to wounding might have been reshuffled over evolution.

Evolution of wound-activated regeneration pathways in the plant kingdom

“…MpERF15, another ERF-type TF that is immediately activated upon wounding and that is crucial for gemmaling regeneration after tissue incision, is a key factor that activates an oxylipin biosynthesis amplification loop in response to wounding, which ultimately triggers cell division and regeneration (Fig. 2C) (Liang et al, 2022). The expression of MpERF15 is dependent on MpCOI1, whereas MpERF15 controls the expression of genes involved in oxylipin production, thereby acting both upstream and downstream of the MpCOI1 oxylipin receptor.…”

“…The expression of MpERF15 is dependent on MpCOI1, whereas MpERF15 controls the expression of genes involved in oxylipin production, thereby acting both upstream and downstream of the MpCOI1 oxylipin receptor. The increased endogenous oxylipin dn-OPDA levels in MpERF15 overexpression lines lead to an increased gemma cell number and apical notch organogenesis, resulting in highly disordered and compact thalli (Liang et al, 2022).…”

“…Interestingly, cross species complementation analysis suggests that MpERF15 is the functional homolog of Arabidopsis ERF109. This TF that belongs to the ERF subfamily X is JA-dependently expressed, controls the expression of auxin biosynthesis-related genes and is essential for wounding-induced regeneration (Cai et al, 2014;Liang et al, 2022;Zhang et al, 2019a;Zhou et al, 2019). Compared with MpERF15, the transcriptional response of the above-mentioned MpERF20/LAXR gene after wounding is relatively late, and the reduced induction of MpERF20/LAXR in loss-of-function Mperf15 ko mutants after wounding suggests that MpERF20/LAXR might operate downstream of MpERF15 (Ishida et al, 2022;Liang et al, 2022).…”

“…Molecular work has pinpointed many key factors in the regeneration process. In particular, members of the ERF TF subfamily X (ERF108 to ERF115) have been implicated with wound signaling and play important roles in the regeneration process during evolution (Heyman et al, 2018;Liang et al, 2022). Upon chirurgical removal of the root tip, a crucial crosstalk between JA and auxin signaling was discovered, being under control of ERF109, a direct target of the JA signaling pathway (Fig.…”

“…Exploring how age affects plant cell fate and regenerative potential, and the development of an efficient regeneration system are essential research areas in plant tissue culture. To our current understanding, the subfamily X ERF members serve as a proxy for the wound signal to activate downstream gene expression, and distinct sets of ERFs may induce diverse regeneration processes, as well as act as a hub for the integration of age-and wounddependent signaling for root regeneration (Canher et 2020;Canher et al, 2022;Heyman et al, 2018;Heyman et al, 2016;Heyman et al, 2013;Liang et al, 2022;Ye et al, 2020).…”