WIND1 Promotes Shoot Regeneration through Transcriptional Activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis

Abstract

Many plant species display remarkable developmental plasticity and regenerate new organs after injury. Local signals produced by wounding are thought to trigger organ regeneration but molecular mechanisms underlying this control remain largely unknown. We previously identified an AP2/ERF transcription factor WOUND INDUCED DEDIFFERENTIATION1 (WIND1) as a central regulator of wound-induced cellular reprogramming in plants. In this study, we demonstrate that WIND1 promotes callus formation and shoot regeneration by upregulating the expression of the ENHANCER OF SHOOT REGENERATION1 (ESR1) gene, which encodes another AP2/ERF transcription factor in Arabidopsis thaliana. The esr1 mutants are defective in callus formation and shoot regeneration; conversely, its overexpression promotes both of these processes, indicating that ESR1 functions as a critical driver of cellular reprogramming. Our data show that WIND1 directly binds the vascular system-specific and wound-responsive cis-element-like motifs within the ESR1 promoter and activates its expression. The expression of ESR1 is strongly reduced in WIND1-SRDX dominant repressors, and ectopic overexpression of ESR1 bypasses defects in callus formation and shoot regeneration in WIND1-SRDX plants, supporting the notion that ESR1 acts downstream of WIND1. Together, our findings uncover a key molecular pathway that links wound signaling to shoot regeneration in plants.

Wounding Triggers Callus Formation via Dynamic Hormonal and Transcriptional Changes

“…9). Interestingly, plt357 mutants as well as WIND1-SRDX and esr1 are not defective in developing calli on CIM, although their calli fail to regenerate shoots on shoot-inducing media (Kareem et al, 2015;Iwase et al, 2017). These observations suggest that these regulators play distinct roles in different contexts, i.e.…”

“…9). We have recently shown that both ARR1-, ARR12-mediated cytokinin signaling and WIND1-mediated wound signaling activate ESR1 expression to promote callus formation at wound sites (Iwase et al, 2017). Thus, these hormonal and transcriptional pathways likely converge and/or cross talk to promote wound-induced callus formation, and future studies should reveal the complex functional relationships between these pathways.…”

“…7). Importantly, ESR1 does not regulate the expression of PLT3, PLT5, and PLT7 (Iwase et al, 2017); thus, they may function in a pathway independent from the WIND1-ESR1-mediated pathway (Fig. 9).…”

“…WIND1 likely mediates wound-induced up-regulation of cytokinin signaling, because woundinduced cytokinin signaling is suppressed in WIND1-SRDX plants. A recent study showed that WIND1 directly up-regulates the expression of ENHANCER OF SHOOT REGENERATION1 (ESR1), encoding another AP2/ERF transcription factor in Arabidopsis, to promote callus formation and shoot regeneration (Iwase et al, 2017). The loss-of-function mutants of WINDs or ESR1 do not completely lack the ability to form calli, suggesting that there are other parallel regulatory pathways of callus formation.…”

Type-B ARABIDOPSIS RESPONSE REGULATORs Specify the Shoot Stem Cell Niche by Dual Regulation of WUSCHEL

“…Six decades ago, Skoog and Miller found that under the induction of exogenous cytokinin and auxin, adventitious shoots could be induced in vitro from a mass of proliferating cells named callus (Skoog and Miller, 1957;Sugimoto et al, 2010;Iwase et al, 2011). This process is defined as de novo shoot regeneration and provides an ideal system for studying the specification of stem cell niche in plants (Duclercq et al, 2011;Iwase et al, 2017). During shoot regeneration, WUS expression promotes cell fate transition from callus cells to OC, which is essential for the specification of the shoot stem cell niche and the subsequent establishment of the shoot meristem (Duclercq et al, 2011;Aichinger et al, 2012;Ikeuchi et al, 2016).…”