To Be or Not to Be? Are Reactive Oxygen Species, Antioxidants, and Stress Signalling Universal Determinants of Life or Death?

Abstract

In the environmental and organism context, oxidative stress is complex and unavoidable. Organisms simultaneously cope with a various combination of stress factors in natural conditions. For example, excess light stress is accompanied by UV stress, heat shock stress, and/or water stress. Reactive oxygen species (ROS) and antioxidant molecules, coordinated by electrical signalling (ES), are an integral part of the stress signalling network in cells and organisms. They together regulate gene expression to redirect energy to growth, acclimation, or defence, and thereby, determine cellular stress memory and stress crosstalk. In plants, both abiotic and biotic stress increase energy quenching, photorespiration, stomatal closure, and leaf temperature, while toning down photosynthesis and transpiration. Locally applied stress induces ES, ROS, retrograde signalling, cell death, and cellular light memory, then acclimation and defence responses in the local organs, whole plant, or even plant community (systemic acquired acclimation, systemic acquired resistance, network acquired acclimation). A simplified analogy can be found in animals where diseases vs. fitness and prolonged lifespan vs. faster aging, are dependent on mitochondrial ROS production and ES, and body temperature is regulated by sweating, temperature-dependent respiration, and gene regulation. In this review, we discuss the universal features of stress factors, ES, the cellular production of ROS molecules, ROS scavengers, hormones, and other regulators that coordinate life and death.

Reactive oxygen species: Multidimensional regulators of plant adaptation to abiotic stress and development

“…Numerous studies have shown that SOD activity markedly increases when plants encounter various abiotic stresses, such as high light, drought, and metal toxicity. SOD activity is often positively correlated with plant tolerance against environmental stress (Szechyńska-Hebda et al, 2022a).…”

“…The resulting damage has negative effects on plant growth, development, and ultimately survival. Thus, maintaining a balance between the generation and detoxification of ROS is vital for normal cellular functions (Szechyńska-Hebda et al, 2022a).…”

“…1 O 2 forms in photosynthetic membranes from reactions between triplet‐state chlorophyll ( 3 chl*) molecules and molecular oxygen (Mittler, 2002). Under neutral conditions, the 1 O 2 concentration is estimated to be ~10 −13 M, the minimum level causing cell membrane damage is ~10 −8 M, while a local concentration of ~10 −5 –10 −4 M often leads to cell death (Kaur and Anastasio, 2017; Szechyńska‐Hebda et al, 2022a). Due to the short lifetime of 1 O 2 (~4 μs) in living cells, 1 O 2 can diffuse over only a short distance (~10–250 nm) from its production site (Szechyńska‐Hebda et al, 2022a).…”

“…Under neutral conditions, the 1 O 2 concentration is estimated to be ~10 −13 M, the minimum level causing cell membrane damage is ~10 −8 M, while a local concentration of ~10 −5 –10 −4 M often leads to cell death (Kaur and Anastasio, 2017; Szechyńska‐Hebda et al, 2022a). Due to the short lifetime of 1 O 2 (~4 μs) in living cells, 1 O 2 can diffuse over only a short distance (~10–250 nm) from its production site (Szechyńska‐Hebda et al, 2022a). The production of 1 O 2 is enhanced under light stress conditions, and lipoxygenase activity can provide an additional source of 1 O 2 (Dogra et al, 2018).…”

“…For example, the level of H 2 O 2 increased to above 3 μmol g −1 /FW by external abscisic acid (ABA) treatment in leaves of maize seedlings by colorimetry assay (Jiang and Zhang, 2001). Indeed, H 2 O 2 ‐mediated signaling is based on an increase in its local concentration to ~10 –4 M in plants (Hao et al, 2014; Szechyńska‐Hebda et al, 2022a). Chemically, H 2 O 2 acts as a weak acid that is highly stable (with a lifetime of >1 ms) and diffusible (with a spread distance over 1 μm, a standard distance between organelles, which function as relay stations).…”