Reactive oxygen species (ROS) play a dual role in plant biology acting on the one hand as important signal transduction molecules and on the other as toxic by-products of aerobic metabolism that ...accumulate in cells during different stress conditions. Because of their toxicity as well as their important signaling role, the level of ROS in cells is tightly controlled by a vast network of genes termed the 'ROS gene network'. Using mutants deficient in key ROS-scavenging enzymes, we have defined a signaling pathway that is activated in cells in response to ROS accumulation. Interestingly, many of the key players in this pathway, including different zinc finger proteins and WRKY transcription factors, are also central regulators of abiotic stress responses involved in temperature, salinity and osmotic stresses. Here, we describe our recent findings and discuss how ROS integrate different signals originating from different cellular compartments during abiotic stress.
• Background Heat shock transcription factors (Hsfs) are modular transcription factors encoded by a large gene family in plants. They bind to the consensus sequence ‘nGAAnnTCCn’ found in the ...promoters of many defence genes, and are thought to function as a highly redundant and flexible gene network that controls the response of plants to different environmental stress conditions, including biotic and abiotic stresses. Hsf proteins encoded by different genes exhibit a high degree of complexity in their interactions. They can potentially bind and activate their own promoters, as well as the promoters of other members of their gene family, and they can form homo- or heterotrimers resulting in altered nuclear localization, as well as enhanced or suppressed transcription. • Scope In this review, we summarize recent studies on Hsf function in Arabidopsis and tomato and present evidence obtained from microarray expression studies in Arabidopsis that the Hsf gene network is highly flexible and specialized, with specific members and/or member combinations controlling the response of plants to particular stress conditions. In addition, we describe recent studies that support the hypothesis that certain Hsfs function as molecular sensors that directly sense reactive oxygen species (ROS) and control the expression of oxidative stress response genes during oxidative stress.
Stress in plants could be defined as any change in growth condition(s) that disrupts metabolic homeostasis and requires an adjustment of metabolic pathways in a process that is usually referred to as ...acclimation. Metabolomics could contribute significantly to the study of stress biology in plants and other organisms by identifying different compounds, such as by-products of stress metabolism, stress signal transduction molecules or molecules that are part of the acclimation response of plants. These could be further tested by direct measurements, correlated with changes in transcriptome and proteome expression and confirmed by mutant analysis. In this review, we will discuss recent application of metabolomics and system biology to the area of plant stress response. We will describe approaches such as metabolic profiling and metabolic fingerprinting as well as combination of different 'omics' platforms to achieve a holistic view of the plant response stress and conduct detailed pathway analysis.
•Rapid systemic signaling is essential for plant acclimation to abiotic stresses.•Waves of Ca2+ and ROS mediate systemic cell-to-cell communication in plants.•Electric signals may facilitate the rate ...of the Ca2+ and ROS wave pathway.•A model for the integration of the Ca2+ and ROS waves is presented.
Systemic signaling pathways enable multicellular organisms to prepare all of their tissues and cells to an upcoming challenge that may initially only be sensed by a few local cells. They are activated in plants in response to different stimuli including mechanical injury, pathogen infection, and abiotic stresses. Key to the mobilization of systemic signals in higher plants are cell-to-cell communication events that have thus far been mostly unstudied. The recent identification of systemically propagating calcium (Ca2+) and reactive oxygen species (ROS) waves in plants has unraveled a new and exciting cell-to-cell communication pathway that, together with electric signals, could provide a working model demonstrating how plant cells transmit long-distance signals via cell-to-cell communication mechanisms. Here, we summarize recent findings on the ROS and Ca2+ waves and outline a possible model for their integration.
► Reactive oxygen species (ROS) play a key signal transduction role in cells. ► The level of ROS in cells is controlled by the ROS gene network. ► Respiratory burst oxidase homologues (RBOHs) are key ...signaling nodes in the ROS network. ► RBOHs regulate a large number of important biological processes in plants. ► RBOHs integrate a multitude of signal transduction pathways with ROS signaling.
Reactive oxygen species (ROS) play a key signal transduction role in cells. They are involved in the regulation of growth, development, responses to environmental stimuli and cell death. The level of ROS in cells is determined by interplay between ROS producing pathways and ROS scavenging mechanisms, part of the ROS gene network of plants. Recent studies identified respiratory burst oxidase homologues (RBOHs) as key signaling nodes in the ROS gene network of plants integrating a multitude of signal transduction pathways with ROS signaling. The ability of RBOHs to integrate calcium signaling and protein phosphorylation with ROS production, coupled with genetic studies demonstrating their involvement in many different biological processes in cells, places RBOHs at the center of the ROS network of cells and demonstrate their important function in plants.
Being sessile organisms, plants evolved sophisticated acclimation mechanisms to cope with abiotic challenges in their environment. These are activated at the initial site of exposure to stress, as ...well as in systemic tissues that have not been subjected to stress (termed systemic acquired acclimation SAA). Although SAA is thought to play a key role in plant survival during stress, little is known about the signaling mechanisms underlying it. Here, we report that SAA in plants requires at least two different signals: an autopropagating wave of reactive oxygen species (ROS) that rapidly spreads from the initial site of exposure to the entire plant and a stress-specific signal that conveys abiotic stress specificity. We further demonstrate that SAA is stress specific and that a temporal—spatial interaction between ROS and abscisic acid regulates rapid SAA to heat stress in plants. In addition, we demonstrate that the rapid ROS signal is associated with the propagation of electric signals in Arabidopsis thaliana. Our findings unravel some of the basic signaling mechanisms underlying SAA in plants and reveal that signaling events and transcriptome and metabolome reprogramming of systemic tissues in response to abiotic stress occur at a much faster rate than previously envisioned.
Cell-to-cell communication and long-distance signaling play a key role in the response of plants to pests, mechanical wounding, and extreme environmental conditions. Here, we report on a rapid ...systemic signal in Arabidopsis thaliana that traveled at a rate of 8.4 centimeters per minute and was dependent on the respiratory burst oxidase homolog D (RbohD) gene. Signal propagation was accompanied by the accumulation of reactive oxygen species (ROS) in the extracellular spaces between cells and was inhibited by the suppression of ROS accumulation at locations distant from the initiation site. The rapid systemic signal was triggered by wounding, heat, cold, high-intensity light, and salinity stresses. Our results reveal the profound role that ROS play in mediating rapid, long-distance, cell-to-cell propagating signals in plants.
Reactive oxygen species (ROS) play a key signaling role in plants and are controlled in cells by a complex network of ROS metabolizing enzymes found in several different cellular compartments. To ...study how different ROS signals, generated in different cellular compartments, are integrated in cells, we generated a double mutant lacking thylakoid ascorbate peroxidase (tylapx) and cytosolic ascorbate peroxidase1 (apx1). Our analysis suggests that two different signals are generated in plants lacking cytosolic APX1 or tylAPX. The lack of a chloroplastic hydrogen peroxide removal enzyme triggers a specific signal in cells that results in enhanced tolerance to heat stress, whereas the lack of a cytosolic hydrogen peroxide removal enzyme triggers a different signal, which results in stunted growth and enhanced sensitivity to oxidative stress. When the two signals are coactivated in cells (i.e. tylapx/apx1), a new response is detected, suggesting that the integration of the two different signals results in a new signal that manifests in late flowering, low protein oxidation during light stress, and enhanced accumulation of anthocyanins. Our results demonstrate a high degree of plasticity in ROS signaling in Arabidopsis (Arabidopsis thaliana) and suggest the existence of redundant pathways for ROS protection that compensate for the lack of classical ROS removal enzymes such as cytosolic and chloroplastic APXs. Further investigation of the enhanced heat tolerance in plants lacking tylAPX, using mutants deficient in chloroplast-to-nuclei retrograde signaling, suggests the existence of a chloroplast-generated stress signal that enhances basal thermotolerance in plants.
Climate change has created an environment where heat stress conditions are becoming more frequent as temperatures continue to raise in crop production areas around the world. This situation leads to ...decreased crop production due to plant sensitivity to heat stress. Reproductive success is critically dependent on plants’ ability to produce functional pollen grains, which are the most thermo-sensitive tissue. Flavonols are plant secondary metabolites known for their potent antioxidative activity, essential for male fertility in several species including tomato, and implicated in heat stress tolerance. Since flavonols are highly abundant in fruits of the tomato
high pigment 2
(
hp2
) mutant, we tested the level of flavonols in pollen of this mutant, under the hypothesis that increased accumulation of flavonols would render pollen more tolerant to heat stress. Indeed, pollen from two alleles of the
hp2
mutant was found to have flavonols levels increased by 18 and 280% compared with wild-type (WT) under moderate chronic heat stress (MCHS) conditions. This mutant produced on average 7.8-fold higher levels of viable pollen and displayed better germination competence under heat stress conditions. The percentage of fully seeded fruits and the number of seeds per fruit were maintained in the mutant under heat stress conditions while decreased in wild-type plants. Our results strongly suggest that increased concentrations of pollen flavonols enhance pollen thermotolerance and reproductive success under heat stress conditions. Thus, the high flavonols trait may help frame the model for improving crop resilience to heat stress.
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