Friend or foe? Reactive oxygen species production, scavenging and signaling in plant response to environmental stresses

Highlights

• Biotic and abiotic stresses induce ROS production in different subcellular compartments.

• In plant cells, different ROS have various degrees of reactivity toward molecules.

• ROS scavengers keep ROS homeostasis and are involved in ROS-dependent signaling.

• Within a cell, ROS cross talk with RNS, hormones, and Ca²⁺ ions.

• ROS transduce SAA signal together with NPQ, hormones, Ca²⁺ and electrical waves.

Abstract

In the natural environment, plants are exposed to a variety of biotic and abiotic stress conditions that trigger rapid changes in the production and scavenging of reactive oxygen species (ROS). The production and scavenging of ROS is compartmentalized, which means that, depending on stimuli type, they can be generated and eliminated in different cellular compartments such as the apoplast, plasma membrane, chloroplasts, mitochondria, peroxisomes, and endoplasmic reticulum. Although the accumulation of ROS is generally harmful to cells, ROS play an important role in signaling pathways that regulate acclimatory and defense responses in plants, such as systemic acquired acclimation (SAA) and systemic acquired resistance (SAR). However, high accumulations of ROS can also trigger redox homeostasis disturbance which can lead to cell death, and in consequence, to a limitation in biomass and yield production. Different ROS have various half-lifetimes and degrees of reactivity toward molecular components such as lipids, proteins, and nucleic acids. Thus, they play different roles in intra- and extra-cellular signaling. Despite their possible damaging effect, ROS should mainly be considered as signaling molecules that regulate local and systemic acclimatory and defense responses. Over the past two decades it has been proven that ROS together with non-photochemical quenching (NPQ), hormones, Ca²⁺ waves, and electrical signals are the main players in SAA and SAR, two physiological processes essential for plant survival and productivity in unfavorable conditions.

Introduction

Reactive oxygen species (ROS) are reactive forms of molecular oxygen, including singlet oxygen (¹O₂), superoxide radical (O₂⁻), hydrogen peroxide (H₂O₂) and hydroxyl radical (OH⁻). In the classical view, they emerged on Earth along with atmospheric oxygen around 2.5 billion years ago and since then have accompanied all of aerobic life [1]. However, oxygen and water were produced in the Universe during supernova explosion, long before rocky planets like Earth were shaped [2]. Moreover, many anaerobic organisms also generate ROS and are equipped with ROS scavenging systems [3]. Therefore, the evolution of both prokaryotic and eukaryotic organisms could proceed in the presence of ROS long before an oxygenic atmosphere appeared. This left an imprint in all kingdoms of life in the context of multiple ROS functions. In physiological conditions they are indispensable for proper cellular metabolism, regulating processes such as cell proliferation, differentiation, signaling reactions, and the ultimate end of the cell cycle, namely the programmed cell death [4], [5], [6], [7].

Contrary to animals, plants demonstrate a sessile life habit and their developmental program is to some extent indeterminate, which means that it is more flexible and dependent on the growing conditions. In this context, ROS are excellent signaling molecules regulating plant metabolic pathways in the proximity of stimuli, but also in the more distal tissues and organs. However, their production and accumulation must be strictly controlled because of their high reactivity and toxicity in higher concentrations.

The origin of programmed cell death in plant and animal kingdoms is common, so as are some morphological and biochemical features such as chromatin condensation, nuclear DNA fragmentation, mitochondria swelling, and plasma membrane collapse [8]. Programmed cell death is conserved in both kingdoms, but plants and animals evolved different, specific mechanisms. In animals, mitochondria and plasma membrane-bound NADPH oxidases are the major source of ROS, playing a central role in the induction of cell death [9]. As opposed to animals, in plant cells ROS are generated in different subcellular compartments, mainly in the chloroplasts and peroxisomes, but also in the mitochondria, plasma membrane, cell wall, endoplasmic reticulum and nuclei [10], [11].

In plants, programmed cell death onset can be the consequence of genetically conserved, developmental processes involved in the formation tracheary elements during xylem differentiation, root cap shedding, generation of perforated leaves, both female and male germline formation, and seed development and germination [12], [13], [14]. However, programmed cell death also constitutes a natural process of replacing old cells by new ones or can be caused by external factors. In the natural environment, plants are simultaneously exposed to a variety of unfavorable conditions, including both biotic and abiotic factors. Biotic stress takes place in response to the invasion of living organisms such as insects, parasites, fungi, bacteria or viruses, while abiotic stress is caused by the negative impact of inanimate nature, such as excessive irradiation, UV radiation, the ozone, drought, flooding, or either low or high temperatures. All of these adverse conditions lead to ROS homeostasis disturbance in plant cells, which in turn evokes acclimatory responses such as systemic acquired acclimation (SAA) and systemic acquired resistance (SAR) [4], [15], [16], [17].