Losing the Warning Signal: Drought Compromises the Cross-Talk of Signaling Molecules in Quercus ilex Exposed to Ozone

Abstract

Understanding the interactions between drought and acute ozone (O3) stress in terms of signaling molecules and cell death would improve the predictions of plant responses to climate change. The aim was to investigate whether drought stress influences the responses of plants to acute episodes of O3 exposure. In this study, the behavior of 84 Mediterranean evergreen Quercus ilex plants was evaluated in terms of cross-talk responses among signaling molecules. Half of the sample was subjected to drought (20% of the effective daily evapotranspiration, for 15 days) and was later exposed to an acute O3 exposure (200 nL L-1 for 5 h). First, our results indicate that in well-water conditions, O3 induced a signaling pathway specific to O3-sensitive behavior. Second, different trends and consequently different roles of phytohormones and signaling molecules (ethylene, ET; abscisic acid, ABA; salycilic acid, SA and jasmonic acid, JA) were observed in relation to water stress and O3. A spatial and functional correlation between these signaling molecules was observed in modulating O3-induced responses in well-watered plants. In contrast, in drought-stressed plants, these compounds were not involved either in O3-induced signaling mechanisms or in leaf senescence (a response observed in water-stressed plants before the O3-exposure). Third, these differences were ascribable to the fact that in drought conditions, most defense processes induced by O3 were compromised and/or altered. Our results highlight how Q. ilex plants suffering from water deprivation respond differently to an acute O3 episode compared to well-watered plants, and suggest new effect to be considered in plant responses to environmental changes. This poses the serious question as to whether or not multiple high-magnitude O3 events (as predicted) can change these cross-talk responses, thus opening it up possible further investigations.

The Role of Salicylic Acid in Plants Exposed to Heavy Metals

“…Under physiological conditions, ROS play a multitude of signaling roles in plants, as well as in other organisms and they take part in a finely-tuned and well-orchestrated regulatory network [72,73]. ROS are indeed integrated into a complex regulatory system in plants which encompasses ROS, plant hormones (e.g., ethylene (ET) and abscisic acid (ABA)), signaling molecules (e.g., salicylic acid (SA) and jasmonic acid (JA)), and secondary messengers (e.g., Ca 2+ ) [74,75]. However, when ROS production exceeds the physiological levels, their accumulation can lead to oxidative stress in the cells, that cause lipids peroxidation, macromolecular degradation, membrane disruption, DNA breakage, and ion leakage in plants [70,74,75].…”

“…ROS are indeed integrated into a complex regulatory system in plants which encompasses ROS, plant hormones (e.g., ethylene (ET) and abscisic acid (ABA)), signaling molecules (e.g., salicylic acid (SA) and jasmonic acid (JA)), and secondary messengers (e.g., Ca 2+ ) [74,75]. However, when ROS production exceeds the physiological levels, their accumulation can lead to oxidative stress in the cells, that cause lipids peroxidation, macromolecular degradation, membrane disruption, DNA breakage, and ion leakage in plants [70,74,75]. For instance, Kaur et al [76] explored Pb-induced ultrastructural changes in roots of wheat and concluded that Pb inhibited root growth, caused ROS generation, and disrupted mitochondrial and nuclear integrity in the tested plant.…”

Interactive effects of changing stratospheric ozone and climate on tropospheric composition and air quality, and the consequences for human and ecosystem health

“…In a study on the Mediterranean oak, Quercus ilex, damage from acute (5-h) exposure of 400 µg m -3 O3 differed between well-watered and water-deprived plants. 171 The normal response to O3, such as release of phytohormones and signaling molecules, ethylene, abscisic acid, salicylic acid, and jasmonic acid, were observed in watered plants but not in water-deprived plants. Thus, interactions between tropospheric O3 and drought are likely to decrease protective responses in plants and make them more susceptible to damage from O3 alone.…”

Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

“…Combination of eO 3 and drought causes reduced increase in SA levels relatively to SA levels resulting from exposure to single stress (Cotrozzi et al, 2017). Hormone-mediated mechanisms of stress acclimation are therefore likely to be sensitive to complex interferences of climate change-related factors.…”

“…Given the contribution of SA toward plant defenses against biotic stresses (Halim, Vess, Scheel, & Rosahl, 2006), SA accumulation during abiotic stresses could be beneficial for plant defenses against pathogens. SA production upon exposure to abiotic stresses is biphasic, with two successive peaks of SA production, as occurs during pathogen attacks (Cotrozzi et al, 2017), thus suggesting that biotic and abiotic stresses cause SA accumulation through similar F I G U R E 5 Effects of climate changerelated stressors and factors on salicylate biosynthesis and biotic stress tolerance. Various climate change-related stresses and environmental factors converge on the modulation of salicylate biosynthesis (Noctor & Mhamdi, 2017;Ogawa et al, 2005;Pál et al, 2014;Sawada et al, 2006;Yalpani et al, 1994).…”