When Bad Guys Become Good Ones: The Key Role of Reactive Oxygen Species and Nitric Oxide in the Plant Responses to Abiotic Stress

Abstract

The natural environment of plants is composed of a complex set of abiotic stresses and their ability to respond to these stresses is highly flexible and finely balanced through the interaction between signaling molecules. In this review, we highlight the integrated action between reactive oxygen species (ROS) and reactive nitrogen species (RNS), particularly nitric oxide (NO), involved in the acclimation to different abiotic stresses. Under stressful conditions, the biosynthesis transport and the metabolism of ROS and NO influence plant response mechanisms. The enzymes involved in ROS and NO synthesis and scavenging can be found in different cells compartments and their temporal and spatial locations are determinant for signaling mechanisms. Both ROS and NO are involved in long distances signaling (ROS wave and GSNO transport), promoting an acquired systemic acclimation to abiotic stresses. The mechanisms of abiotic stresses response triggered by ROS and NO involve some general steps, as the enhancement of antioxidant systems, but also stress-specific mechanisms, according to the stress type (drought, hypoxia, heavy metals, etc.), and demand the interaction with other signaling molecules, such as MAPK, plant hormones, and calcium. The transduction of ROS and NO bioactivity involves post-translational modifications of proteins, particularly S-glutathionylation for ROS, and S-nitrosylation for NO. These changes may alter the activity, stability, and interaction with other molecules or subcellular location of proteins, changing the entire cell dynamics and contributing to the maintenance of homeostasis. However, despite the recent advances about the roles of ROS and NO in signaling cascades, many challenges remain, and future studies focusing on the signaling of these molecules in planta are still necessary.

Keywords: S-glutathionylation; S-nitrosylation; crosstalk; gene expression; signaling; systemic acquired acclimation.

FIGURE 1

Main sources of nitric oxide (NO) and reactive oxygen species (ROS) in plant cells (adapted from Groß et al., 2013).

FIGURE 2

Schematic representation showing the interplay between NO, ROS, and other signaling molecules in response to abiotic stress. The signaling molecules include hormones, mitogen-activated protein kinases (MAPKs), cyclic guanosine monophosphate (cGMP), cyclic adenosine diphosphoribose (cADPR) and calcium (Ca²⁺). Besides the interaction with components of signaling pathways, NO and ROS also transmit signals via post-translational modifications in proteins [metal nitrosylation, tyrosine nitration, S-nitrosylation, and oxidative post-translational modifications (Ox-PTM)]. ROS degradation by antioxidants and NO storage (GSNO, S-nitrosoglutathione) and degradation by GSNOR (GSNO reductase) and THB (truncated hemoglobin) are demonstrated. Arrows and T-bars indicate activation and inhibition, respectively (adapted from Oz et al., 2015).