Signaling Toward Reactive Oxygen Species-Scavenging Enzymes in Plants

Abstract

Reactive oxygen species (ROS) are signaling molecules essential for plant responses to abiotic and biotic stimuli as well as for multiple developmental processes. They are produced as byproducts of aerobic metabolism and are affected by adverse environmental conditions. The ROS content is controlled on the side of their production but also by scavenging machinery. Antioxidant enzymes represent a major ROS-scavenging force and are crucial for stress tolerance in plants. Enzymatic antioxidant defense occurs as a series of redox reactions for ROS elimination. Therefore, the deregulation of the antioxidant machinery may lead to the overaccumulation of ROS in plants, with negative consequences both in terms of plant development and resistance to environmental challenges. The transcriptional activation of antioxidant enzymes accompanies the long-term exposure of plants to unfavorable environmental conditions. Fast ROS production requires the immediate mobilization of the antioxidant defense system, which may occur via retrograde signaling, redox-based modifications, and the phosphorylation of ROS detoxifying enzymes. This review aimed to summarize the current knowledge on signaling processes regulating the enzymatic antioxidant capacity of plants.

Keywords: antioxidant enzymes; calcium; mitogen-activated protein kinases; oxidative stress; plants; reactive oxygen species; signaling; stress.

Figure 1

MAPK-dependent regulation of antioxidant enzymes during plant stress responses. Most left pathway shows the universal order of a MAP3K/MAP2K/MAPK cascade. Solid arrows indicate induction, dashed arrows show phosphorylation, and ⊥ indicates negative regulation. Question mark means an unknown component of the pathway. ABA, abscisic acid; ANPs, Arabidopsis nucleus- and phragmoplast-localized kinases; AP2/ERF6, Apetala2/Ethylene-responsive element binding factor 6; APX, ascorbate peroxidase; CAT, catalase; CSD, Cu/Zn superoxide dismutase; DHAR, dehydroascorbate reductase; ERF104, Ethylene-responsive element binding factor 104; FSD, Fe superoxide dismutase; GR, glutathione reductase; HSFA4A, Heat shock transcription factor A4A; MAPK, mitogen-activated protein kinase; MAP2K, mitogen-activated protein kinase kinase; MAP3K, mitogen-activated protein kinase kinase kinase; MSD, Mn superoxide dismutase; RLCKs, receptor-like cytoplasmic kinases; RLKs, receptor-like kinases; ROS, reactive oxygen species; SA, salicylic acid.

Figure 2

Graphical (A) and tabular (B) overview of common transcription factors (TFs) predicted to regulate the expression of FSD1, APX1, and DHAR1 under the regulation of mitogen-activated protein kinases.

Figure 3

Mechanisms of Ca²⁺-mediated regulation of antioxidant enzymes during stress in plants. Solid arrows indicate induction, and dashed arrows show phosphorylation. Question mark means an unknown regulation. APX, ascorbate peroxidases; CAT, catalase; CPK, Ca²⁺-dependent protein kinases; DHAR, dehydroascorbate reductase; GPX, glutathione peroxidase; GR, glutathione reductase; MDHAR, monodehydroascorbate reductase; SOD, superoxide dismutase; ZmCCaM, Ca²⁺/calmodulin-dependent protein kinase from Zea mays.

Figure 4

Reactive nitrogen species-mediated direct regulation of antioxidant enzymes during plant stress responses. Solid arrows indicate induction, and ⊥ indicates negative regulation. APX, ascorbate peroxidase; CAT, catalase; FSD, Fe superoxide dismutase; MDHAR, monodehydroacorbate reductase; MSD, Mn superoxide dismutase.

Figure 5

In vivo subcellular localization of FSD1-GFP in plastids, nuclei and cytoplasm of 4-day-old Arabidopsis fsd1-1 mutant harboring proFSD1::FSD1:GFP construct (Dvořák et al., 2020) as revealed by confocal laser scanning microscope equipped with an Airyscan detector. (A) Pavement cells of leaf epidermis; (B) epidermal cells of hypocotyl; (C) lateral root cap cells; (D) root meristematic cells. n, nucleus; p, plastid; s, stromule. Scale bars: (A, C, D) 10 μm; (B) 20 μm.

Figure 6

Overview of direct and indirect mechanisms of antioxidant enzyme regulation in response to stress-induced ROS generation.