Sensing of heat, high light (HL), or mechanical injury by a single leaf of a plant results in the activation of different systemic signals that reach systemic tissues within minutes and trigger ...systemic acquired acclimation (SAA) or systemic wound responses (SWRs), resulting in a heightened state of stress readiness of the entire plant. Among the different signals associated with rapid systemic responses to stress in plants are electric, calcium, and reactive oxygen species (ROS) waves. These signals propagate from the stressed or injured leaf to the rest of the plant through the plant vascular bundles, and trigger SWRs and SAA in systemic tissues. However, whether they can propagate through other cell types, and whether or not they are interlinked, remain open questions. Here we report that in response to wounding or heat stress (HS), but not HL stress, the ROS wave can propagate through mesophyll cells of Arabidopsis (Arabidopsis thaliana). Moreover, we show that ROS production by mesophyll cells during these stresses is sufficient to restore SWR and SAA transcript accumulation in systemic leaves, as well as SAA to HS (but not HL). We further show that propagation of the ROS wave through mesophyll cells could contribute to systemic signal integration during HL and HS stress combination. Our findings reveal that the ROS wave can propagate through tissues other than the vascular bundles of plants, and that different stresses can trigger different types of systemic signals that propagate through different cell layers and induce stress-specific systemic responses.
• 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.
Temperature stress can have a devastating effect on plant metabolism, disrupting cellular homeostasis, and uncoupling major physiological processes. A direct result of stress‐induced cellular changes ...is the enhanced accumulation of toxic compounds in cells that include reactive oxygen species (ROS). Although a considerable amount of work has shown a direct link between ROS scavenging and plant tolerance to temperature stress, recent studies have shown that ROS could also play a key role in mediating important signal transduction events. Thus, ROS, such as superoxide (O2–), are produced by NADPH oxidases during abiotic stress to activate stress‐response pathways and induce defense mechanisms. The rates and cellular sites of ROS production during temperature stress could play a central role in stress perception and protection. ROS levels, as well as ROS signals, are thought to be controlled by the ROS gene network of plants. It is likely that in plants this network is interlinked with the different networks that control temperature stress acclimation and tolerance. In this review paper, we attempt to summarize some of the recent studies linking ROS and temperature stress in plants and propose a model for the involvement of ROS in temperature stress sensing and defense.
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.
Many studies have described the response mechanisms of plants to salinity and heat applied individually; however, under field conditions some abiotic stresses often occur simultaneously. Recent ...studies revealed that the response of plants to a combination of two different stresses is specific and cannot be deduced from the stresses applied individually. Here, we report on the response of tomato plants to a combination of heat and salt stress. Interestingly, and in contrast to the expected negative effect of the stress combination on plant growth, our results show that the combination of heat and salinity provides a significant level of protection to tomato plants from the effects of salinity. We observed a specific response of plants to the stress combination that included accumulation of glycine betaine and trehalose. The accumulation of these compounds under the stress combination was linked to the maintenance of a high K⁺ concentration and thus a lower Na⁺/K⁺ ratio, with a better performance of the cell water status and photosynthesis as compared with salinity alone. Our findings unravel new and unexpected aspects of the response of plants to stress combination and provide a proposed list of enzymatic targets for improving crop tolerance to the abiotic field environment.
Abiotic stresses such as drought, heat or salinity are major causes of yield loss worldwide. Recent studies have revealed that the acclimation of plants to a combination of different environmental ...stresses is unique and therefore cannot be directly deduced from studying the response of plants to each of the different stresses applied individually. The efficient detoxification of reactive oxygen species (ROS) is thought to play a key role in enhancing the tolerance of plants to abiotic stresses. Here, we report on the role of melatonin in the protection of the photosynthetic apparatus through the increase in ROS detoxification in tomato plants grown under the combination of salinity and heat, two of the most common abiotic stresses known to act jointly. Plants treated with exogenous melatonin showed a different modulation in the expression on some antioxidant-related genes and their related enzymes. More specifically, ascorbate peroxidase, glutathione reductase, glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase (APX, GR, GPX and Ph-GPX, resepctively) showed an antagonistic regulation as compared to plants that did not receive melatonin. This translated into a better antioxidant capacity and to a lesser ROS accumulation under stress combination. The performance of the photosynthesis parameters and the photosystems was also increased in plants treated with exogenous melatonin under the combination of salinity and heat. In accordance with these findings, tomato plants treated with melatonin were found to grow better under stress combination that the non-treated ones. Our study highlights the important role that exogenous melatonin plays in the acclimation of plants to a combination of two different abiotic stresses, and how this compound can specifically regulate oxidative stress-related genes and enzymes to increase plant tolerance.
Abscisic acid (ABA) plays a key role in plant acclimation to abiotic stress. Although recent studies suggested that ABA could also be important for plant acclimation to a combination of abiotic ...stresses, its role in this response is currently unknown. Here we studied the response of mutants impaired in ABA signalling (abi1-1) and biosynthesis (aba1-1) to a combination of water deficit and heat stress. Both mutants displayed reduced growth, biomass, and survival when subjected to stress combination. Focusing on abi1-1, we found that although its stomata had an impaired response to water deficit, remaining significantly more open than wild type, its stomatal aperture was surprisingly reduced when subjected to the stress combination. Stomatal closure during stress combination in abi1-1 was accompanied by higher levels of H₂O₂ in leaves, suggesting that H₂O₂ might play a role in this response. In contrast to the almost wild-type stomatal closure phenotype of abi1-1 during stress combination, the accumulation of ascorbate peroxidase 1 and multiprotein bridging factor 1c proteins, required for acclimation to a combination of water deficit and heat stress, was significantly reduced in abi1-1. Our findings reveal a key function for ABA in regulating the accumulation of essential proteins during a combination of water deficit and heat stress.
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