Ozone and Reactive Oxygen Species

Abstract

High tropospheric ozone (O3) concentrations affect plant growth and crop yield. O3 enters leaves through stomata and rapidly degrades in the apoplast into other reactive oxygen species (ROS), which readily interact with surrounding biomolecules. Due to their high reactivity, ROS act as important signalling molecules. Apoplastic ROS perception induces secondary ROS production in other cellular compartments and activates interorganelle signalling pathways towards stress defence. Defence responses include activation of hormonal signalling, the enhancement of antioxidative defence responses, protection of the photosynthetic machinery and induction of cell death processes. Different species prioritise different defence strategies and population studies towards the identification of genetic loci associated with O3 tolerance are currently the most promising approach for identifying genes involved in O3 tolerance.

Key Concepts

  • While the stratospheric O3 layer has protective UV‐B screening properties, tropospheric O3 accumulation near the earth's surface is a health hazard to living organisms.
  • Ozone enters through open stomatal pores in the leaf epidermis and triggers rapid ROS accumulation and complex signalling pathways originating from the apoplastic space between cells.
  • Acute O3 exposure in sensitive plants results in visible cell death lesions; long‐term chronic exposures to O3 levels above 40 ppb leads to a reduction in crop yields due to reduced photosynthesis and disruption to metabolism.
  • The photosynthetic activity decreases under O3 exposure and subsequently causes a reduction in CO2 fixation and central carbohydrate metabolism. Subsequently, catabolic processes are enhanced to re‐mobilise resources, causing early senescence and a shift in source‐sink relations.
  • ROS are continuously produced during photosynthesis and respiration and ROS production increases under stress conditions. This serves as an important signalling mechanism that initiates defence and acclimation processes.
  • ROS, calcium and hormones accumulate within different intra‐ and extracellular compartments and act together as signals in a dense and complex signalling network under stress conditions.
  • Stomatal closure physically blocks the entry of air pollutants or pathogens. Stomatal closure is a defence response, triggered by O3 and other types of abiotic and biotic stress, measured through stomatal conductance (gs).
  • While harsh stress results in passive cell death, programmed cell death (PCD) is an active defence mechanism that can isolate and contain the spread of diseases to smaller areas of tissue in the plant.
  • Strategies to increase the tolerance of plants to O3 include population studies, transgenic approaches as well as the application of protective chemicals.

Keywords: reactive oxygen species (ROS); plant stress response; pollution; ozone; plant signalling

Figure 1. Global distribution of tropospheric O3. Global maps of OMI/MLS tropospheric ozone Aura O3 Monitoring Instrument (OMI) in combination with Aura Microwave Limb Sounder (MLS). Image from http://acd‐ext.gsfc.nasa.gov/Data_services/cloud_slice/gif/May16.gif. NASA tropospheric O3 concentrations, monthly average May 16th 2016. Where 40 ppb tropospheric O3 concentrations or more are associated with crop damage.
Figure 2. Ozone‐induced signaling pathways and components. Once O3 enters the apoplastic space through open stomata this is followed by a series of events. (1) O3 sensing in the apoplast and signal transduction into the cytosol via still unidentified mechanisms: (a) receptor like kinases (RLKs), (b) redox‐sensitive membrane‐bound proteins, (c) ROS transport across membranes through channels such as aquaporins, (d) membrane lipid oxidation, (2) The first biphasic ROS burst occurs in the chloroplast; (3) rapid stomatal closure defence response; (4) Second ROS burst in the apoplast via MAPK triggered phosphorylation of NADPH oxidases that generates apoplastic superoxide. (5) Downstream signalling events on PCD (HR and senescence) and acclimation via SIMR such as reduced growth and increased defence. ‘P’ surrounded by red circle indicates activation of membrane protein through phosphorylation. Purple indicates redox regulation or ROS scavenging capability. Dotted arrows indicate hypothetical pathways, solid arrows indicate connections supported by experimental evidence. ROS, reactive oxygen species; Ca2+, calcium molecules; CPK, cysteine protein kinases; NADPH oxidase, nicotinaminde adenine dinucleotide phosphate oxidase; SLAC1, slow anion channel 1; MAPK, mitogen‐activated protein kinase; O2, oxygen; O2, superoxide; H2O2, hydrogen peroxide; ABA, abscisic acid; SIMR, stress‐induced morphological response; HR, hypersensitive response; RLK, receptor‐like kinase; AsA, ascorbate; DHA, dehydroascorbate; GST, glutathione‐S‐transferase; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GSH, glutathione; GSSG, oxidised glutathione.
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Krasensky, Julia, Carmody, Melanie, Sierla, Maija, and Kangasjärvi, Jaakko(Mar 2017) Ozone and Reactive Oxygen Species. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001299.pub3]