Epidermal Cell Death in Rice Is Confined to Cells with a Distinct Molecular Identity and Is Mediated by Ethylene and H2O2 through an Autoamplified Signal Pathway

Abstract

Rice (Oryza sativa) forms adventitious root primordia at stem nodes during normal development. Root emergence is preceded by ethylene-induced, H2O2-mediated local death of epidermal cells. Exogenous H2O2 or enhancement of endogenous H2O2 promoted epidermal cell death in a dose-dependent manner. Inhibition of NADPH oxidase lowered ethylene-induced cell death rates. Inhibition of ethylene perception by 1-methylcyclopropene did not abolish H2O2-induced cell death, indicating that H2O2 acts downstream of ethylene. Microarray studies of epidermal cells that undergo cell death identified 61 genes coregulated by the ethylene-releasing compound ethephon and by H2O2, supporting a joint signaling pathway. Regulation of the ethylene biosynthetic genes 1-Aminocyclopropane-1-Carboxylate Oxidase1 and Ethylene Overproducer-Like1 and downregulation of Metallothionein2b (MT2b), which encodes a reactive oxygen scavenger, indicated mutual enhancement of ethylene and H2O2 signaling. Analysis of MT2b knockdown mutants showed that cell death rates were inversely related to MT2b transcript abundance. Epidermal cells above adventitious roots have a morphological and molecular identity distinct from other epidermal cells. Pro-death signals regulated several transcription factor genes with a proposed function in cell type specification. It is hypothesized that induction of cell death is dependent on epidermal cell identity.

Waterproofing Crops: Effective Flooding Survival Strategies

“…This cell-to-cell mechanosignaling enabled emergence of the adventitious root. Remarkably, comparison of the transcriptomes of epidermal cells located directly above the primordium with those nearby indicated that there was spatial priming of programmed cell death prior to its elicitation (Steffens and Sauter, 2009). The mRNAs enriched above the subtending primordium were associated with ethylene biosynthesis, whereas the depleted transcripts included one encoding a metallothionein that negatively regulates cell death.…”

A Co-Opted Hormonal Cascade Activates Dormant Adventitious Root Primordia upon Flooding in Solanum dulcamara

“…Additional factors, such as hypoxia, might feed into the model presented here but are not essential for reactivation of the primordia. An important distinction between the S. dulcamara and rice models for AR reactivation is the target tissue: while in rice the epidermal cells are the main target of the ethylene-dependent activation pathway (Steffens and Sauter, 2009), AR dormancy does not seem to depend on mechanical restriction by the epidermis in S. dulcamara. (Supplemental Fig.…”

“…The well-described mechanism for flooding-induced breaking of AR primordia dormancy in rice involves hydrogen peroxide-dependent epidermal cell death, resulting in removal of the physical restriction to primordium growth (Steffens and Sauter, 2009). In S. dulcamara, the mechanism is fundamentally different, as AR primordia are located much deeper, covered by several layers of cortex cells (Fig.…”

“…The authors therefore suggested a hormonal model in which the balance between the positive, synergistic action of ethylene and GA and the inhibitory action of ABA regulates the process of epidermal cell death and AR emergence (Steffens et al, 2006). Ethylene and hydrogen peroxide promote epidermal cell death by coregulating a small set of genes (Steffens and Sauter, 2009). Among these, metallothionein MT2b was down-regulated, and this was shown to be sufficient to induce cell death.…”

Ethylene and hydrogen peroxide are involved in hypoxia signaling that modulatesAtERF73/HRE1expression

“…Higher plants are aerobic organisms that suffer serious physical damage and rapidly die when oxygen availability is limited because of soil flooding. [1][2][3][4] Low oxygen shifts energy metabolism from aerobic to anaerobic, which in turn adversely affects nutrient and water uptake. Under oxygendeficient conditions, production of both hydrogen peroxide (H 2 O 2 ) and ethylene is triggered by hypoxia signaling.…”