The roles of reactive oxygen metabolism in drought: not so cut and dried

Abstract

Drought is considered to cause oxidative stress, but the roles of oxidant-induced modifications in plant responses to water deficit remain obscure. Key unknowns are the roles of reactive oxygen species (ROS) produced at specific intracellular or apoplastic sites and the interactions between the complex, networking antioxidative systems in restricting ROS accumulation or in redox signal transmission. This Update discusses the physiological aspects of ROS production during drought, and analyzes the relationship between oxidative stress and drought from different but complementary perspectives. We ask to what extent redox changes are involved in plant drought responses and discuss the roles that different ROS-generating processes may play. Our discussion emphasizes the complexity and the specificity of antioxidant systems, and the likely importance of thiol systems in drought-induced redox signaling. We identify candidate drought-responsive redox-associated genes and analyze the potential importance of different metabolic pathways in drought-associated oxidative stress signaling.

Figure 1.

Current concepts of how drought increases the generation of ROS in photosynthesis. A, Cartoon of leaf section in well-watered plants in which relatively high intercellular CO₂ concentrations (C_i) allow efficient regeneration of terminal oxidants and limit RuBP oxygenation. B, Drought-induced stomatal closure restricts CO₂ uptake, favoring photorespiratory production of H₂O₂ in the peroxisome (1) and possibly favoring production of superoxide and H₂O₂ (2) or singlet oxygen (3) by the photosynthetic electron transport chain. PGA, 3-Phosphoglyceric acid. [See online article for color version of this figure.]

Figure 2.

Multiple ROS-producing enzymes at the cell surface/exterior. Enzymes are shown in blue and their redox cofactors are indicated in yellow. Class III peroxidases may accept electrons from several types of compounds to generate superoxide, but in many cases their physiological reductant is not established (O’Brien et al., 2012). [See online article for color version of this figure.]

Figure 3.

The 15 of the 302 redox-linked genes that respond >2-fold in the same direction in both drought 1 and drought 2 data sets and their response in related conditions. Data extracted from Genevestigator are shown as log₂ values compared with controls. Red and green indicate induction and repression. Genes are ordered from the top according to the number of conditions in which they respond. The full list of genes and their expression values is given in Supplemental Table S1. For details of experiments, see Supplemental Table S2. [See online article for color version of this figure.]

Figure 4.

Peroxide-removing enzymes: roles as antioxidants, in signaling, or both? Cartoon of the best characterized peroxide-metabolizing enzymes in plants. Other mechanisms are possible and for ease of display reactions are not shown stoichiometrically. 2CPRX, 2-cys-PRX; ASC, ascorbate; DHAR, dehydroascorbate reductase; MDHAR, monodehydroascorbate reductase; NTR, NADPH-thioredoxin C; PRXII, PRX type II; ROH, water or organic alcohol; ROOH, H₂O₂ or organic peroxide; S, sulfur atom in disulfide bond; SH, sulfhydryl (thiol) group; SOH, sulfenic acid group. [See online article for color version of this figure.]

Figure 5.

Analysis of drought-inducible gene expression in responses to redox perturbation. A, Heatmap of drought-induced genes extracted from Genevestigator and the response of these genes to ABA or oxidative stress (top) and histogram showing expression of oxidative stress marker genes after the different treatments (bottom). Data are shown as log₂ values compared with Col-0 (the wild type or untreated). Experimental details are given in Supplemental Table S2. Red and green on the heatmap indicate induction and repression according to the color scale shown at the top. The five genes for which data are shown in the bottom histogram are as follows (left to right): APX1, GSTU24, UGT75B1, UGT73B5, and GPX6 (for values, see Supplemental Table S3C). B, Overlap of induced genes (cutoff, 2-fold) in the two drought experiments; 375 genes were induced >2-fold in at least one of the experiments (Supplemental Table S3A). C, The number of these 375 genes that were induced >2-fold by the different oxidative stresses (indicated in red circles within the outer blue circles). Col-0, Ecotype Columbia 0 of Arabidopsis. [See online article for color version of this figure.]