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.

Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress

“…In submerged plant tissues the limited gas diffusion causes passive ethylene accumulation. This rapid ethylene build-up can occur prior to the onset of severe hypoxia, making it a timely and reliable signal for submergence 4,5 . In several plant species, ethylene regulates adaptive responses to flooding involving morphological and anatomical modifications that prevent hypoxia 5 .…”

Oxygen Sensing and Integrative Stress Signaling in Plants

“…Arabidopsis contains 10 NADPH oxidases, called RBOHs, of which three-RBOHD, RBOHF, and RBOHI-have been implicated in low-oxygen responses (Pucciariello et al, 2012;Liu et al, 2017;Lin et al, 2017). Although fermentative genes including ADH1 have been shown to depend on single RBOH activity, the exact mechanism through which each RBOH contributes to low-oxygen signaling needs further investigation.…”

“…Changes in the internal concentration of oxygen, but also e.g. ethylene, are crucial early signals for the initiation of adaptation strategies to flooding (Sasidharan and Voesenek, 2015;Sasidharan et al, 2017). Initially, a plant cell responds to nearly all these different types of stresses by using the same set of second messengers (such as reactive oxygen species [ROS], calcium, nitric oxide [NO], and lipid molecules) and by activating signaling cascades through kinases (Bjornson et al, 2016;Zhu, 2016).…”

The Dynamic Plant: Capture, Transformation, and Management of Energy

“…The latter catalyze the first step in ERF-VII turnover through oxidation of an evolutionarily conserved N-terminal Cys to a Cys-sulfonic acid residue (White et al, 2017). Nitric oxide also is important in the conditional regulation of ERF-VII abundance (Giuntoli and Perata, 2018;Sasidharan et al, 2018;Wagner et al, 2018).…”

“…The Update by Sasidharan et al (2018) surveys signatures of gaseous signals (O 2 , CO 2 , ethylene, and nitric oxide), as well as ROS for flooding conditions, including soil waterlogging and complete submergence. When gas exchange with the atmosphere is limited, the constitutive production of ethylene ensures a robust early signal of coming limitations in O 2 as well as CO 2 .…”