Ozone responses in Arabidopsis: beyond stomatal conductance.

Luis O Morales,Dmitry Yarmolinsky,Alexey Shapiguzov,Hannes Kollist,Johanna Leppälä,Mikael Brosché,Lauri Vaahtera,Omid Safronov

doi:10.1093/plphys/kiab097

Abstract

Tropospheric ozone (O3) is a major air pollutant that decreases yield of important crops worldwide. Despite long-lasting research of its negative effects on plants, there are many gaps in our knowledge on how plants respond to O3. In this study, we used natural variation in the model plant Arabidopsis (Arabidopsis thaliana) to characterize molecular and physiological mechanisms underlying O3 sensitivity. A key parameter in models for O3 damage is stomatal uptake. Here we show that the extent of O3 damage in the sensitive Arabidopsis accession Shahdara (Sha) does not correspond with O3 uptake, pointing toward stomata-independent mechanisms for the development of O3 damage. We compared tolerant (Col-0) versus sensitive accessions (Sha, Cvi-0) in assays related to photosynthesis, cell death, antioxidants, and transcriptional regulation. Acute O3 exposure increased cell death, development of lesions in the leaves, and decreased photosynthesis in sensitive accessions. In both Sha and Cvi-0, O3-induced lesions were associated with decreased maximal chlorophyll fluorescence and low quantum yield of electron transfer from Photosystem II to plastoquinone. However, O3-induced repression of photosynthesis in these two O3-sensitive accessions developed in different ways. We demonstrate that O3 sensitivity in Arabidopsis is influenced by genetic diversity given that Sha and Cvi-0 developed accession-specific transcriptional responses to O3. Our findings advance the understanding of plant responses to O3 and set a framework for future studies to characterize molecular and physiological mechanisms allowing plants to respond to high O3 levels in the atmosphere as a result of high air pollution and climate change.

Highlights

Plants are continuously exposed to adverse environmental conditions that impair growth and fitness (Suzuki et al, 2014)
We associated O3 sensitivity in Cvi and other Arabidopsis accessions with more open stomata leading to high O3 uptake (Broscheet al., 2010)
Here we show that O3 sensitivity in Sha is not because of increased stomatal conductance or high O3 uptake (Figure 2)

Summary

Introduction

Plants are continuously exposed to adverse environmental conditions that impair growth and fitness (Suzuki et al, 2014). Ozone (O3) is a phytotoxic air pollutant that reduces the yield of important crops worldwide (Ainsworth et al, 2012). O3 enters the plant through stomata and in the apoplast it breaks down into reactive oxygen species (ROS), such as superoxide (O–2 ) and hydrogen peroxide (H2O2; Ainsworth, 2017; Waszczak et al, 2018). Depending on the O3 concentration, sensitive plant species activate cell death programs leading to the development of lesions (Broscheet al., 2010; Langebartels et al, 2002). O3 and most abiotic and biotic stresses increase the formation of ROS with potentially deleterious toxic effects on DNA, proteins, lipids, and carbohydrates. ROS are not merely damaging molecules, as they initiate signaling events that help plants acclimate to stress (Jaspers and Kangasjarvi, 2010; Waszczak et al, 2018)

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