Reactive Oxygen Species in Plant Signaling Waszczak, Cezary; Carmody, Melanie; Kangasjärvi, Jaakko
Annual review of plant biology,
04/2018, Letnik:
69, Številka:
1
Journal Article
Recenzirano
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As fixed organisms, plants are especially affected by changes in their environment and have consequently evolved extensive mechanisms for acclimation and adaptation. Initially considered by-products ...from aerobic metabolism, reactive oxygen species (ROS) have emerged as major regulatory molecules in plants and their roles in early signaling events initiated by cellular metabolic perturbation and environmental stimuli are now established. Here, we review recent advances in ROS signaling. Compartment-specific and cross-compartmental signaling pathways initiated by the presence of ROS are discussed. Special attention is dedicated to established and hypothetical ROS-sensing events. The roles of ROS in long-distance signaling, immune responses, and plant development are evaluated. Finally, we outline the most challenging contemporary questions in the field of plant ROS biology and the need to further elucidate mechanisms allowing sensing, signaling specificity, and coordination of multiple signals.
Reactive oxygen species (ROS) are known to accumulate during abiotic stresses, and different cellular compartments respond to them by distinctive profiles of ROS formation. In contrast to earlier ...views, it is becoming increasingly evident that even during stress, ROS production is not necessarily a symptom of cellular dysfunction but might represent a necessary signal in adjusting the cellular machinery to the altered conditions. ROS can modulate many signal transduction pathways, such as mitogen-activated protein kinase cascades, and ultimately influence the activity of transcription factors. However, the picture of ROS-mediated signaling is still fragmentary and the issues of ROS perception as well as the signaling specificity remain open. Here, we review some of the recent advances in plant abiotic stress signaling with emphasis on processes known to be affected heavily by ROS.
Guard cells form stomatal pores that optimize photosynthetic carbon dioxide uptake with minimal water loss. Stomatal movements are controlled by complex signaling networks that respond to ...environmental and endogenous signals. Regulation of stomatal aperture requires coordinated activity of reactive oxygen species (ROS)-generating enzymes, signaling proteins, and downstream executors such as ion pumps, transporters, and plasmamembrane channels that control guard cell turgor pressure. Accumulation of ROS in the apoplast and chloroplasts is among the earliest hallmarks of stomatal closure. Subsequent increase in cytoplasmic Ca2+ concentration governs the activity of multiple kinases that regulate the activity of ROS-producing enzymes and ion channels. In parallel, ROS directly regulate the activity of multiple proteins via oxidative posttranslational modifications to fine-tune guard cell signaling. In this review, we summarize recent advances in the role of ROS in stomatal closure and discuss the importance of ROS in regulation of signal amplification and specificity in guard cells.
Plants grow and reproduce within a highly dynamic environment that can see abrupt changes in conditions, such as light intensity, temperature, humidity, or interactions with biotic agents. Recent ...studies revealed that plants can respond within seconds to some of these conditions, engaging many different metabolic and molecular networks, as well as rapidly altering their stomatal aperture. Some of these rapid responses were further shown to propagate throughout the entire plant via waves of reactive oxygen species (ROS) and Ca2+ that are possibly mediated through the plant vascular system. Here, we propose that the integration of these signals is mediated through pulses of gene expression that are coordinated throughout the plant in a systemic manner by the ROS/Ca+2 waves.
Recent studies reveal that plants respond within the seconds to minutes time-scale to different biotic and/or abiotic stimuli.
The rapid response of plants to different stimuli spans many metabolic, molecular, and biochemical pathways, and involves genes essential for plant acclimation or defense.
Stomata can respond within minutes to different stimuli, such as ozone, pathogen infection, or light stress, and this response can be propagated from the affected leaf to different systemic leaves by the ROS/Ca2+ wave.
Different transcriptional regulators display a triphasic expression pattern with transient peaks of expression at the seconds, minutes and hours time-scale. These regulators may shape the acclimation and/or defense response of plants in pulses of gene expression that orchestrate the gene response network.
Rapid responses and the rapid systemic signaling pathways they activate could coordinate the systemic response of plants to a combination of different environmental conditions, enhancing the overall acclimation and ability of plants to withstand the rapidly changing conditions within their environment.
•ROS production is strictly regulated and integrated with other signaling networks in plants.•Calcium has a critical role in ROS signaling and the control of ROS production.•Extracellular ROS ...production originates from different sources that have non-overlapping roles.•Intracellular ROS perception is provided by parallel systems of oxidative protein modification and redox status monitoring.•NPR1 serves as a central intracellular integrator of ROS, nitric oxide and salicylic acid signaling pathways.
Reactive oxygen species are recognized as important signaling components in a wide range of processes in plants and most other organisms. Reactive oxygen species are produced in different subcellular compartments in response to specific stimuli and the production is under tight control in order to avoid detrimental side-effects. Calcium signaling, protein phosphorylation and other signaling pathways are intimately involved in the control and coordination of reactive oxygen production. Any signal that should result in a specific response must eventually be perceived. Direct redox modification of transcription factors and other proteins are critical for the perception of intracellular reactive oxygen species; however, sensing of their extracellular counterparts awaits elucidation.
Plant signalling in acute ozone exposure VAINONEN, JULIA P; KANGASJÄRVI, JAAKKO
Plant, cell and environment,
February 2015, Letnik:
38, Številka:
2
Journal Article
Recenzirano
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Exposure of plants to high ozone concentrations causes lesion formation in sensitive plants. Plant responses to ozone involve fast and massive changes in protein activities, gene expression and ...metabolism even before any tissue damage can be detected. Degradation of ozone and subsequent accumulation of reactive oxygen species (ROS) in the extracellular space activates several signalling cascades, which are integrated inside the cell into a fine‐balanced network of ROS signalling. Reversible protein phosphorylation and degradation plays an important role in the regulation of signalling mechanisms in a complex crosstalk with plant hormones and calcium, an essential second messenger. In this review, we discuss the recent advances in understanding the molecular mechanisms of ozone uptake, perception and signalling pathways activated during the early steps of ozone response, and discuss the use of ozone as a tool to study the function of apoplastic ROS in signalling.
Stomata, the pores formed by a pair of guard cells, are the main gateways for water transpiration and photosynthetic CO2 exchange, as well as pathogen invasion in land plants. Guard cell movement is ...regulated by a combination of environmental factors, including water status, light, CO2 levels and pathogen attack, as well as endogenous signals, such as abscisic acid and apoplastic reactive oxygen species (ROS). Under abiotic and biotic stress conditions, extracellular ROS are mainly produced by plasma membrane‐localized NADPH oxidases, whereas intracellular ROS are produced in multiple organelles. These ROS form a sophisticated cellular signaling network, with the accumulation of apoplastic ROS an early hallmark of stomatal movement. Here, we review recent progress in understanding the molecular mechanisms of the ROS signaling network, primarily during drought stress and pathogen attack. We summarize the roles of apoplastic ROS in regulating stomatal movement, ABA and CO2 signaling, and immunity responses. Finally, we discuss ROS accumulation and communication between organelles and cells. This information provides a conceptual framework for understanding how ROS signaling is integrated with various signaling pathways during plant responses to abiotic and biotic stress stimuli.
Stomata are the main gateways for water transpiration and photosynthetic CO2 exchange, as well as pathogen invasion in land plants. Stomatal movement is regulated by a combination of environmental factors including water status, light, CO2 levels and pathogen attack, as well as abscisic acid and apoplastic reactive oxygen species (ROS).
Reactive oxygen species (ROS), important signaling molecules in plants, are involved in developmental control and stress adaptation. ROS production can trigger broad transcriptional changes; however, ...it is not clear how specificity in transcriptional regulation is achieved.
A large collection of public transcriptome data from the model plant Arabidopsis thaliana is available for analysis. These data can be used for the analysis of biological processes that are associated with ROS signaling and for the identification of suitable transcriptional indicators. Several online tools, such as Genevestigator and Expression Angler, have simplified the task to analyze, interpret, and visualize this wealth of data.
The analysis of the exact transcriptional responses to ROS requires the production of specific ROS in distinct subcellular compartments with precise timing, which is experimentally difficult. Analyses are further complicated by the effect of ROS production in one subcellular location on the ROS accumulation in other compartments. In addition, even subtle differences in the method of ROS production or treatment can lead to significantly different outcomes when various stimuli are compared.
Due to the difficulty of inducing ROS production specifically with regard to ROS type, subcellular localization, and timing, we propose that the concept of a "ROS marker gene" should be re-evaluated. We suggest guidelines for the analysis of transcriptional data in ROS signaling. The use of "ROS signatures," which consist of a set of genes that together can show characteristic and indicative responses, should be preferred over the use of individual marker genes.
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