•High ozone concentrations affect plant metabolism and development.•Epicuticular waxes, cell wall and plasma membrane are O3-sensing localizations.•Early O3-signaling components are directly ...connected to the O3-sensing sites.•Promising tracks to elucidate putative early O3 signaling components are proposed.
All along their life, plants and trees are exposed to various stresses, and particularly to abiotic ones. Ozone (O3) is one of the most important air pollutants, whose ground levels keep increasing as a result of climate change. High O3 concentrations deeply affect plants and cells, and impact worldwide crop and forest production. In plant leaves, O3 directly interferes with surface tissues or reaches mesophyll cells through stomata. In this case, O3 is almost immediately degraded into reactive oxygen species (ROS) in the apoplastic space of plant cells. For plants to acclimate to O3, the O3 stress signal has to be perceived at the cellular level and relayed to the nucleus to lead to cell reprogramming. The aim of this review is to focus on different O3-sensing localizations, i.e., epicuticular waxes, the cell wall and the plasma membrane, and to detail the different early signaling components related to these sites – in particular lipids, membrane proteins (G proteins, NADPH oxidases and ion channels) and MAP kinases. Finally, some interesting putative membrane-related O3 signaling components are presented as clues to be validated in future investigations.
SUMMARY
Tree growth and survival are dependent on their ability to perceive signals, integrate them, and trigger timely and fitted molecular and growth responses. While ectomycorrhizal symbiosis is a ...predominant tree‐microbe interaction in forest ecosystems, little is known about how and to what extent it helps trees cope with environmental changes. We hypothesized that the presence of Laccaria bicolor influences abiotic cue perception by Populus trichocarpa and the ensuing signaling cascade. We submitted ectomycorrhizal or non‐ectomycorrhizal P. trichocarpa cuttings to short‐term cessation of watering or ozone fumigation to focus on signaling networks before the onset of any physiological damage. Poplar gene expression, metabolite levels, and hormone levels were measured in several organs (roots, leaves, mycorrhizas) and integrated into networks. We discriminated the signal responses modified or maintained by ectomycorrhization. Ectomycorrhizas buffered hormonal changes in response to short‐term environmental variations systemically prepared the root system for further fungal colonization and alleviated part of the root abscisic acid (ABA) signaling. The presence of ectomycorrhizas in the roots also modified the leaf multi‐omics landscape and ozone responses, most likely through rewiring of the molecular drivers of photosynthesis and the calcium signaling pathway. In conclusion, P. trichocarpa‐L. bicolor symbiosis results in a systemic remodeling of the host's signaling networks in response to abiotic changes. In addition, ectomycorrhizal, hormonal, metabolic, and transcriptomic blueprints are maintained in response to abiotic cues, suggesting that ectomycorrhizas are less responsive than non‐mycorrhizal roots to abiotic challenges.
Significance Statement
Current research on tree physiology primarily focuses on tree responses to abiotic stress, with little emphasis on root‐associated mutualistic fungi. Our results provide insights into how and to what extent the presence of ectomycorrhizas modifies host responses to abiotic changes: symbiosis has local and systemic impacts on host signaling pathways. A better understanding of the molecular mechanisms underpinning root‐microbe mutualistic interactions under abiotic stress will allow for robust modeling of tree adaptation to environmental challenges.
Plants are frequently exposed to adverse environmental conditions such as drought and ozone (O3). Under these conditions, plants can survive due to their ability to adjust their metabolism. The aim ...of the present study was to compare the detoxification mechanisms of three oak species showing different O3 sensitivity and water use strategy. Two-year-old seedlings of Quercus ilex, Q. pubescens and Q. robur were grown under the combination of three levels of O3 (1.0, 1.2 and 1.4 times the ambient O3 concentration) and three levels of water availability (on average 100, 80 and 42% of field capacity i.e. well-watered, moderate drought and severe drought, respectively) in an O3 Free Air Controlled Exposure facility. Ozone and drought induced the accumulation of reactive oxygen species (ROS) and this phenomenon was species-specific. Sometimes, ROS accumulation was not associated with membrane injury suggesting that several antioxidative defence mechanisms inhibited or alleviated the oxidative damage. Both O3 and drought increased total carotenoids that were able to prevent the peroxidation action by free radicals in Q. ilex, as confirmed by unchanged malondialdehyde by-product values. The concomitant decrease of total flavonoids may be related to the consumption of these compounds by the cell to inhibit the accumulation of hydrogen peroxide. Unchanged total phenols confirmed that Q. ilex has a superior ability to counteract oxidative conditions. Similar responses were found in Q. pubescens, although the negative impact of both factors was less efficiently faced than in the sympatric Q. ilex. In Q. robur, high O3 concentrations and severe drought induced a partial rearrangement of the phenylpropanoid pathways. These antioxidative mechanisms were not able to protect the cell structure (as confirmed by ROS accumulation) suggesting that Q. robur showed a lower degree of tolerance than the other two species.
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•Detoxification mechanisms at the basis of the high plasticity of oak species•Ozone and drought had antagonistic effects on biochemical traits.•Intrinsic physiological and biochemical mechanisms contribute to stress tolerance.
Ozone (O3) and drought increase tree oxidative stress. To protect forest health, we need to improve risk assessment, using metric model such as the phytotoxic O3 dose above a threshold of ...y nmol·m−2·s−1 (PODy), while taking into account detoxification mechanisms and interacting stresses. The impact of drought events on the effect of O3 pollution deserves special attention. Water deficit may decrease O3 entrance into the leaves by reducing stomatal opening; however, water deficit also induces changes in cell redox homeostasis. Besides, the behaviour of the cell antioxidative charge in case of stress combination (water deficit and O3) still remains poorly investigated. To decipher the response of detoxification mechanisms relatively to the Halliwell-Asada-Foyer cycle (HAF), we exposed poplar saplings (Populus nigra × deltoides) composed of two genotypes (Carpaccio and Robusta), to various treatments for 17 days, i.e. i) mild water deficit, ii) 120 ppb O3, and iii) a combination of these two treatments. Ozone similarly impacted the growth of the two genotypes, with an important leaf loss. Water deficit decreased growth by almost one third as compared to the control plants. As for the combined treatment, water deficit protected the saplings from leaf ozone injury, but with an inhibitory effect on growth. The pool of total ascorbate was not modified by the different treatments, while the pool of total glutathione increased with POD0. We noticed a few differences between the two genotypes, particularly concerning the activity of monodehydroascorbate reductase and glutathione reductase relatively to POD0. The expression profiles of genes coding for the dehydroascorbate reductase and glutathione reductase isoforms differed, probably in link with the putative localisation of ROS production in response to water deficit and ozone, respectively. Our result would argue for a major role of MDHAR, GR and glutathione in the preservation of the redox status.
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•Poplar genotypes differed in ascorbate-glutathione regulation as related to POD0 increase.•MDHAR and glutathione might have an important role under ozone conditions.•Antagonistic effects prevailed during the interaction between water deficit and ozone.
In plants, a temperature downshift represents a major stress that will lead to the induction or repression of many genes. Therefore, the cold signal has to be perceived and transmitted to the ...nucleus. In response to a cold exposure, we have shown that the phospholipase D (PLD) and the phospholipase C (PLC)/diacylglycerol kinase pathways are simultaneously activated. The role of these pathways in the cold response has been investigated by analyzing the transcriptome of cold-treated Arabidopsis (Arabidopsis thaliana) suspension cells in the presence of U73122 or ethanol, inhibitors of the PLC/diacylglycerol kinase pathway and of the phosphatidic acid produced by PLD, respectively. This approach showed that the expression of many genes was modified by the cold response in the presence of such agents. The cold responses of most of the genes were repressed, thus correlating with the inhibitory effect of U73122 or ethanol. We were thus able to identify 58 genes that were regulated by temperature downshift via PLC activity and 87 genes regulated by temperature downshift via PLD-produced phosphatidic acid. Interestingly, each inhibitor appeared to affect different cold response genes. These results support the idea that both the PLC and PLD pathways are upstream of two different signaling pathways that lead to the activation of the cold response. The connection of these pathways with the CBF pathway, currently the most understood genetic system playing a role in cold acclimation, is discussed.
Nitrate (NO
) and ammonium (NH
) are prevalent nitrogen (N) sources for plants. Although NH
should be the preferred form of N from the energetic point of view, ammonium nutrition often exhibits ...adverse effects on plant physiological functions and induces an important growth-limiting stress referred as ammonium syndrome. The effective incorporation of NH
into amino acid structures requires high activity of the mitochondrial tricarboxylic acid cycle and the glycolytic pathway. An unavoidable consequence of glycolytic metabolism is the production of methylglyoxal (MG), which is very toxic and inhibits cell growth in all types of organisms. Here, we aimed to investigate MG metabolism in
plants grown on NH
as a sole N source. We found that changes in activities of glycolytic enzymes enhanced MG production and that markedly elevated MG levels superseded the detoxification capability of the glyoxalase pathway. Consequently, the excessive accumulation of MG was directly involved in the induction of dicarbonyl stress by introducing MG-derived advanced glycation end products (MAGEs) to proteins. The severe damage to proteins was not within the repair capacity of proteolytic enzymes. Collectively, our results suggest the impact of MG (mediated by MAGEs formation in proteins) in the contribution to NH
toxicity symptoms in
.
The release of the complete genome sequence of Arabidopsis enabled the largest sucrose synthase family described to date, comprising six distinct members, for which expression profiles were not yet ...available, to be identified. Aimed at understanding the precise function of each AtSUS member among the family, a comparative study of protein structure was performed, together with an expression profiling of the whole gene family using the technique of real-time quantitative reverse transcriptase-polymerase chain reaction. Transcript levels were analysed in several plant organs, including both developing and germinating seeds. A series of treatments such as oxygen deprivation, dehydration, cold treatment, or various sugar feedings were then carried out to characterize the members of the family further. The AtSUS genes exhibit distinct but partially redundant expression profiles. Under anaerobic conditions, for instance, both AtSUS1 and AtSUS4 mRNA levels increase, but in a distinct manner. AtSUS2 is specifically and highly induced in seeds at 12 d after flowering and appears as a marker of seed maturation. AtSUS3 seems to be induced in various organs under dehydration conditions including leaves deprived of water or submitted to osmotic stress as well as late-maturing seeds. AtSUS5 and AtSUS6 are expressed in nearly all plant organs and do not exhibit any transcriptional response to stresses. These results add new insights on the expression of SUS genes and are discussed in relation to distinct functions for each member of the AtSUS family.
Key message
Ozone, one of the major atmospheric pollutants, alters tree growth, mainly by decreasing carbon assimilation and allocation to stems and roots. To date, the mechanisms of O
3
impact at ...the cellular level have been investigated mainly on young trees grown in controlled or semi-controlled conditions. In the context of climate change, it is necessary to introduce a valuable defence parameter in the models that currently predict O
3
impact on mature trees and the carbon sequestration capacity of forest ecosystems.
Context
Air pollution is an important factor that affects negatively forest ecosystems. Among oxidative air pollutants, ozone is considered as the most toxic in terms of impact on vegetation.
Aims
This paper focuses on the negative impacts of ozone on trees in controlled conditions or in their natural environment. The current knowledge of the responses at cell level is presented and ways to improve their use for ozone risk assessment of forest stands are discussed.
Methods
Information was collected from original papers or reviews, providing an overview of the research conducted over the last 60 years.
Results
The negative effects of ozone on carbon assimilation and tree biomass production were reviewed and discussed, with a focus on effects on cell processes implied in cell defence, including stomatal regulation, detoxification, signalling, and biosynthesis of wood compound.
Conclusion
In the context of increasing significance of O
3
flux approach, this review intends to shed light into the black box of defence processes, which are playing a crucial part within the effective O
3
dose modelling. Today, it is recognized that tropospheric ozone inhibits tree growth and its role on the future carbon sink of the forest ecosystem is discussed along with the combination of other environmental factors like elevated temperature, water, and nitrogen supply, likely to be modified in the context of climate change.
The impact of ozone (O3) pollution events on the plant drought response needs special attention because spring O3 episodes are often followed by summer drought. By causing stomatal sluggishness, O3 ...could affect the stomatal dynamic during a subsequent drought event. In this context, we studied the impact of O3 exposure and water deficit (in the presence or in the absence of O3 episode) on the stomatal closure/opening mechanisms relative to irradiance or vapour pressure deficit (VPD) variation. Two genotypes of Populus nigra x deltoides were exposed to various treatments for 21 days. Saplings were exposed to 80 ppb/day O3 for 13 days, and then to moderate drought for 7 days. The curves of the stomatal response to irradiance and VPD changes were determined after 13 days of O3 exposure, and after 21 days in the case of subsequent water deficit, and then fitted using a sigmoidal model. The main responses under O3 exposure were stomatal closure and sluggishness, but the two genotypes showed contrasting responses. During stomatal closure induced by a change in irradiance, closure was slower for both genotypes. Nonetheless, the genotypes differed in stomatal opening under light. Carpaccio stomata opened more slowly than control stomata, whereas Robusta stomata tended to open faster. These effects could be of particular interest, as stomatal impairment was still present after O3 exposure and could result from imperfect recovery. Under water deficit alone, we observed slower stomatal closure in response to VPD and irradiance, but faster stomatal opening in response to irradiance, more marked in Carpaccio. Under the combined treatment, most of the parameters showed antagonistic responses. Our results highlight that it is important to take genotype-specific responses and interactive stress cross-talk into account to improve the prediction of stomatal conductance in response to various environmental modifications.
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•Genotypes differed in stomatal dynamics in response to irradiance or VPD changes.•Ozone induced stomatal closure and sluggishness in response to irradiance changes.•Stomata recovery was not complete after ozone exposure.•Water deficit decreased closing speed but increased opening speed.•Ozone followed by water deficit resulted in an antagonistic effect.
This study indicates that the possible multiple stomatal responses to environmental stimuli must be taken into account in order to better define the parameters of the stomatal conductance model.
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