Abstract
Plant stress signalling involves bursts of reactive oxygen species (ROS), which can be mimicked by the application of acute pulses of ozone. Such ozone-pulses inhibit photosynthesis and trigger stomatal closure in a few minutes, but the signalling that underlies these responses remains largely unknown. We measured changes in Arabidopsis thaliana gas exchange after treatment with acute pulses of ozone and set up a system for simultaneous measurement of membrane potential and cytosolic calcium with the fluorescent reporter R-GECO1. We show that within 1min, prior to stomatal closure, O3 triggered a drop in whole-plant CO2 uptake. Within this early phase, O3 pulses (200-1000ppb) elicited simultaneous membrane depolarization and cytosolic calcium increase, whereas these pulses had no long-term effect on either stomatal conductance or photosynthesis. In contrast, pulses of 5000ppb O3 induced cell death, systemic Ca2+ signals and an irreversible drop in stomatal conductance and photosynthetic capacity. We conclude that mesophyll cells respond to ozone in a few seconds by distinct pattern of plasma membrane depolarizations accompanied by an increase in the cytosolic calcium ion (Ca2+ ) level. These responses became systemic only at very high ozone concentrations. Thus, plants have rapid mechanism to sense and discriminate the strength of ozone signals.
Highlights
Reactive oxygen species (ROS) are important signalling molecules in various plant developmental and stress responses (Mittler, 2017; Waszczak et al, 2018)
This study revealed that acute doses of O3, which do not trigger cell death, cause an immediate depolarization of mesophyll cells in three stages that correlate with cytosolic calcium signals
Whole rosettes of intact Arabidopsis thaliana plants were exposed to 3- or 10-min O3 pulses of 1000 ppb
Summary
Reactive oxygen species (ROS) are important signalling molecules in various plant developmental and stress responses (Mittler, 2017; Waszczak et al, 2018). The superoxide anion (O2À) and hydrogen peroxide (H2O2) form gradients that promote root development, plant immunity, cell death, as well as stomatal movements (Dunand et al, 2007; Tsukagoshi et al, 2010; Kadota et al, 2015; Sierla et al, 2016). The latter response was shown to depend on the leucine-rich-repeat receptor kinase HPCA1, which functions as H2O2 sensor in guard cells that activates calcium ion (Ca2+) channels and subsequent stomatal closure (Wu et al, 2020). We use the tropospheric air pollutant O3 as a proxy to create a burst of apoplastic ROS (Wohlgemuth et al., 2002), to study the earliest steps following ROS perception in mesophyll cells
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