Signal Dynamics and Interactions during Flooding Stress

Abstract

Flooding is detrimental for nearly all higher plants, including crops. The compound stress elicited by slow gas exchange and low light levels under water is responsible for both a carbon and an energy crisis ultimately leading to plant death. The endogenous concentrations of four gaseous compounds, oxygen, carbon dioxide, ethylene, and nitric oxide, change during the submergence of plant organs in water. These gases play a pivotal role in signal transduction cascades, leading to adaptive processes such as metabolic adjustments and anatomical features. Of these gases, ethylene is seen as the most consistent, pervasive, and reliable signal of early flooding stress, most likely in tight interaction with the other gases. The production of reactive oxygen species (ROS) in plant cells during flooding and directly after subsidence, during which the plant is confronted with high light and oxygen levels, is characteristic for this abiotic stress. Low, well-controlled levels of ROS are essential for adaptive signaling pathways, in interaction with the other gaseous flooding signals. On the other hand, excessive uncontrolled bursts of ROS can be highly damaging for plants. Therefore, a fine-tuned balance is important, with a major role for ROS production and scavenging. Our understanding of the temporal dynamics of the four gases and ROS is basal, whereas it is likely that they form a signature readout of prevailing flooding conditions and subsequent adaptive responses.

Figure 1.

Signal dynamics during a typical light-limited flooding event. During early submergence (light gray shading), ethylene accumulates rapidly while oxygen levels decline gradually. Upon hypoxia, NO and ROS bursts occur. Upon recovery from prolonged submergence (dark gray shading), there is transient ethylene (ET) production while oxygen levels return to normal. NO dynamics upon desubmergence are unknown, but a strong ROS burst likely occurs. The schematic conveys general trends based on current knowledge and is intended to show that flooding signals can display strong variability during different phases of the flooding event. Furthermore, these signal dynamics are strongly dependent on flood conditions, plant species, and the organ and tissues affected.

Figure 2.

Overview of the major flooding signals (yellow boxes) and their interactions, leading to the regulation of major adaptive responses (gray boxes). Restricted gas exchange between the plant and its environment during flooding results in alterations in endogenous levels of CO₂, oxygen, and ethylene. These primary signals can further give rise to the secondary signals ROS, NO, and starvation. Changes in the availability of oxygen and CO₂ are the net result of production, consumption, and diffusion and, therefore, are highly dependent on light conditions during flooding. Changes in CO₂ likely influence flooding responses, due to its role as a substrate for photosynthesis. CO₂ limitation in the light leads to starvation and subsequent metabolic reprogramming via energy signaling mechanisms. A decline in oxygen levels limits aerobic respiration but also triggers downstream acclimation responses via the ERFVII transcription factors. Oxygen-dependent stabilization of ERFVIIs via the N-end rule enhances hypoxia-responsive gene expression, including the fermentation enzymes (e.g. ADH). However, an efficient transcriptional induction requires an ERFVII-dependent ROS burst through RBOHD. ROS also is formed nonenzymatically during hypoxia via the ETC. ERFVII degradation also is dependent on NO. Hypoxia induces NO accumulation, probably due to increased NR activity and subsequent nitrite reduction at the mitochondrial ETC. However, NO also is scavenged during hypoxia by hemoglobin (HB1), which, in turn, is induced by ERFVIIs. Oxygen levels also play an essential role in energy homeostasis, not just via their role as a substrate for respiration. The activation of fermentation through hypoxia-stabilized ERFVIIs boosts ATP production, diminishing starvation. At the same time, fermentation is highly dependent on sufficient sugar availability and, thus, is inhibited by starvation. Additionally, NO increase upon hypoxia is suggested to inhibit COX and the tricarboxylic acid cycle enzyme aconitase, altering efficient ATP generation via respiration. Ethylene biosynthesis rates can change upon flooding, but reduced gas exchange is the primary reason for ethylene accumulation to saturating levels. Ethylene accumulation plays a pivotal role in aerenchyma and adventitious root (AR) development mediated by interactions with ROS. PCD of epidermal cells covering AR primordia is required for penetration and is essential in the cortex for aerenchyma formation. Ethylene-mediated ROS accumulation occurs via RBOH activity or due to reduced ROS scavenging.