Abstract
Reactive oxygen species (ROS) have been reported to trigger signaling pathways that interact with other signaling pathways mediated by nitric oxide, lipid messengers, and plant hormones. In a previous study, we demonstrated that ethylene was involved in hypoxia signaling to regulate the expression of downstream genes such as AtERF73/HRE1 and ADH1. Furthermore, H2O2 and ethylene interplay has an effect on AtERF73/HRE1 and ADH1 expression during the early stages of hypoxia signaling. Here, we propose a model for the main transcription factor AtERF73/HRE1, which is controlled by 3 pathways during hypoxia. These include an ethylene-dependent pathway, an ethylene-independent/H2O2-dependent pathway, and an ethylene and H2O2-independent pathway involved in hypoxia signaling to modulate AtERF73/HRE1.
Keywords: ethylene, hydrogen peroxide, reactive oxygen species, ERF, hypoxia
Global climate change is an immediate and important issue, and flooding has become a serious problem, reducing plant survival or impeding plant growth, and causing serious yield losses in crops around the world. Higher plants are aerobic organisms that suffer serious physical damage and rapidly die when oxygen availability is limited because of soil flooding.1-4 Low oxygen shifts energy metabolism from aerobic to anaerobic, which in turn adversely affects nutrient and water uptake. Under oxygen-deficient conditions, production of both hydrogen peroxide (H2O2) and ethylene is triggered by hypoxia signaling.
During hypoxia signaling, ethylene accumulates and plays central roles in regulating the expression of downstream genes such as AtERF73/HRE1 and ADH1 in Arabidopsis. The enzymes involved in ethylene biosynthesis such as ACC synthase (ACS) and ACC oxidase (ACO) have been demonstrated to be induced after hypoxia.5 It was also reported that ethylene regulates aerenchyma formation in the root tips of maize plants exposed to hypoxic conditions.6 In addition to ethylene, an ethylene-independent signal is also required to mediate hypoxic induction of AtERF73/HRE1.7 AtERF73/HRE1 is very similar to the rice Sub1A and SNORKEL genes, which play central roles in the submergence tolerance of lowland and deepwater rice, respectively, and all 3 belong to the group VII ERF (ethylene responsive factor) subfamily.8,9
Low-oxygen conditions can cause accumulation of toxic end products from anaerobic respiration and reactive oxygen species (ROS). H2O2 is generated during hypoxia and has been suggested to act as a signal component that triggers downstream responses in hypoxia signaling.10 H2O2 production has been observed under both anoxia and heat stress, which is involved in the induction of heat shock transcription factor (HSF) and heat shock protein expression.11,12 In our previous study, we demonstrated that H2O2 affected the abundance of AtERF73/HRE1 and ADH1 mRNAs in both wild-type Arabidopsis and the ethylene-insensitive mutant ein2–5. Furthermore, the transcript levels of AtERF73/HRE1 and ADH1 were decreased in both the wild-type and ein2–5 mutant after a combined treatment of hypoxia and diphenyleneiodonium (DPI), which functions as a NADPH oxidase inhibitor to block the production of H2O2.13,14 This implies that H2O2 is not entirely downstream of ethylene. The effects of H2O2 occurred mainly in the early stages of the hypoxia signaling pathways that regulate the expression of AtERF73/HRE1 and ADH1. However, the AtERF73/HRE1 and ADH1 expression levels were not completely repressed after hypoxia combined with DPI treatment. This also implies that H2O2 and ethylene signaling are necessary, but not sufficient, for the control of downstream gene transcription during hypoxic stress. According to our previous results, we propose a model for AtERF73/HRE1 regulation during hypoxia signaling via ethylene and H2O2 interplay (Fig. 1). This model includes an ethylene-dependent pathway, an ethylene-independent/H2O2-dependent pathway, and an ethylene and H2O2-independent pathway. All 3 of these induce AtERF73/HRE1 transcript accumulation. Under the ethylene-dependent pathway, our previous analyses showed that hypoxic induction of several peroxidase and cytochrome P450 genes was enhanced in AtERF73/HRE1-RNAi lines but reduced in ein2–5, suggesting that hypoxia-induced H2O2 accumulation is required for ethylene signaling to modulate this set of peroxidase and cytochrome P450 genes. In addition, AtERF73/HRE1 could inhibit the hypoxic induction of these genes.7,14 Under the ethylene-independent/H2O2-dependent pathway, our results also demonstrated that the effect of H2O2 was not completely dependent on ethylene signaling, suggesting parallel control of the transcription of downstream genes by H2O2 and ethylene signals in hypoxia signaling. The transcript levels of AtERF73/HRE1 and ADH1 were significantly decreased in Col by combined hypoxia and DPI treatments. Furthermore, induction of AtERF73/HRE1 in ein2–5 by hypoxia was significantly decreased by the addition of DPI at the early stage but not at the late stage during hypoxic stress, while the induction levels of ADH1 in ein2–5 were slightly decreased. These results not only demonstrated that H2O2 participates in regulating AtERF73/HRE1 and ADH1 transcription but also implied the presence of an ethylene- and H2O2-independent pathway that regulates AtERF73/HRE1 and ADH1 expression during hypoxic stress.
Figure 1. Model for the involvement of AtERF73/HRE1 and ADH1 transcripts in hypoxia and ethylene-H2O2 mediated pathways. Hypoxia triggers ethylene and H2O2 production, which increases the accumulation of AtERF73/HRE1 transcripts through (I) an ethylene-dependent pathway, (II) an ethylene-independent/H2O2-dependent pathway, and (III) an ethylene/H2O2-independent pathway. AtERF73/HRE1 positively regulates ADH1 genes and negatively regulates a set of peroxidase and cytochrome P450 genes in hypoxia signaling.
To determine how plants sense low oxygen, it is important to understand the early signaling of hypoxia. Here, we propose a model for the interplay between ethylene and H2O2 in AtERF73/HRE1 and ADH1 regulation in the hypoxia pathway to help clarify the roles of ethylene and H2O2 during hypoxic stress.
Acknowledgments
The author greatly thanks Dr Ming-Che Shih (Agricultural Biotechnology Research Center, Academia Sinica, Taiwan) for careful reading of the manuscript.
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