Search

Stress results in the enhanced accumulation of reactive oxygen species (ROS) in plants, altering the redox state of cells and triggering the activation of multiple defense and acclimation mechanisms. In addition to activating ROS and redox responses in tissues that are directly subjected to stress (termed 'local' tissues), the sensing of stress in plants triggers different systemic signals that travel to other parts of the plant (termed 'systemic' tissues) and activate acclimation and defense mechanisms in them; even before they are subjected to stress. Among the different systemic signals triggered by stress in plants are electric, calcium, ROS, and redox waves that are mobilized in a cell-to-cell fashion from local to systemic tissues over long distances, sometimes at speeds of up to several millimeters per second. Here, we discuss new studies that identified various molecular mechanisms and proteins involved in mediating systemic signals in plants. In addition, we highlight recent studies that are beginning to unravel the mode of integration and hierarchy of the different systemic signals and underline open questions that require further attention. Unraveling the role of ROS and redox in plant stress responses is highly important for the development of climate resilient crops.

Systemic acquired acclimation and wound signaling require the transmission of electrical, calcium, and reactive oxygen species (ROS) signals between local and systemic tissues of the same plant. However, whether such signals can be transmitted between two different plants is largely unknown. Here, we reveal a new type of plant-to-plant aboveground direct communication involving electrical signaling detected at the surface of leaves, ROS, and photosystem networks. A foliar electrical signal induced by wounding or high light stress applied to a single dandelion leaf can be transmitted to a neighboring plant that is in direct contact with the stimulated plant, resulting in systemic photosynthetic, oxidative, molecular, and physiological changes in both plants. Furthermore, similar aboveground changes can be induced in a network of plants serially connected via touch. Such signals can also induce responses even if the neighboring plant is from a different plant species. Our study demonstrates that electrical signals can function as a communication link between transmitter and receiver plants that are organized as a network (community) of plants. This process can be described as network-acquired acclimation.

Heat waves occurring during droughts can have a devastating impact on yield, especially if they happen during the flowering and seed set stages of the crop cycle. Global warming and climate change are driving an alarming increase in the frequency and intensity of combined drought and heat stress episodes, critically threatening global food security. Because high temperature is detrimental to reproductive processes, essential for plant yield, we measured the inner temperature, transpiration, sepal stomatal aperture, hormone concentrations and transcriptomic response of closed soybean flowers developing on plants subjected to a combination of drought and heat stress. Here, we report that, during a combination of drought and heat stress, soybean plants prioritize transpiration through flowers over transpiration through leaves by opening their flower stomata, while keeping their leaf stomata closed. This acclimation strategy, termed ‘differential transpiration’, lowers flower inner temperature by about 2–3°C, protecting reproductive processes at the expense of vegetative tissues. Manipulating stomatal regulation, stomatal size and/or stomatal density of flowers could serve as a viable strategy to enhance the yield of different crops and mitigate some of the current and future impacts of global warming and climate change on agriculture.

Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.

Reactive oxygen species (ROS) and the photoreceptor protein phytochrome B (phyB) play a key role in plant acclimation to stress. However, how phyB that primarily functions in the nuclei impacts ROS signaling mediated by respiratory burst oxidase homolog (RBOH) proteins that reside on the plasma membrane, during stress, is unknown. Arabidopsis thaliana and Oryza sativa mutants, RNA-Seq, bioinformatics, biochemistry, molecular biology, and whole-plant ROS imaging were used to address this question. Here, we reveal that phyB and RBOHs function as part of a key regulatory module that controls apoplastic ROS production, stress-response transcript expression, and plant acclimation in response to excess light stress. We further show that phyB can regulate ROS production during stress even if it is restricted to the cytosol and that phyB, respiratory burst oxidase protein D (RBOHD), and respiratory burst oxidase protein F (RBOHF) coregulate thousands of transcripts in response to light stress. Surprisingly, we found that phyB is also required for ROS accumulation in response to heat, wounding, cold, and bacterial infection. Our findings reveal that phyB plays a canonical role in plant responses to biotic and abiotic stresses, regulating apoplastic ROS production, possibly while at the cytosol, and that phyB and RBOHD/RBOHF function in the same regulatory pathway.

Cell-to-cell communication is fundamental to multicellular organisms and unicellular organisms living in a microbiome. A unique cell-to-cell communication mechanism that uses reactive oxygen species (ROS) as a signal (termed the ‘ROS wave’) was recently identified in flowering plants. Here we report that a ROS-mediated cell-to-cell signaling process, like the ROS wave, can be found in ferns, mosses, unicellular algae, amoeba, mammalian cells, and isolated hearts. We further show that this process can be triggered by a localized stress treatment or H2O2 application and blocked by inhibition of NADPH oxidases, and that in unicellular algae, it communicates important stress-response signals between cells. Taken together, our findings suggest that cell-to-cell ROS signaling evolved before unicellular and multicellular organisms diverged. The finding of a ROS wave-like signaling process in mammalian cells further contributes to our understanding of different diseases and could impact the development of new drugs that target cancer or heart disease.

The wounding-induced reactive oxygen species (ROS) wave is accompanied by a systemic whole-plant redox response in Arabidopsis.

A combination of drought and heat stress, occurring at the vegetative or reproductive growth phase of many different crops, can have a devastating impact on yield. In soybean (Glycine max), a considerable effort has been made to develop genotypes with enhanced yield production under conditions of drought or heat stress. However, how these genotypes perform in terms of growth, physiological responses and most importantly seed production, under conditions of drought and heat combination is mostly unknown. Here, we studied the impact of water deficit and heat stress combination on the physiology, seed production and yield per plant of two soybean genotypes, Magellan and Plant Introduction (PI) 548313, that differ in their reproductive responses to heat stress. Our findings reveal that although PI 548313 produced more seeds than Magellan under conditions of heat stress, under conditions of water deficit and heat stress combination its seed production decreased. Because number of flowers and pollen germination of PI 548313 remained high under heat or water deficit and heat combination, the reduced seed production exhibited by PI 548313 under the stress combination could be a result of processes that occur at the stigma, ovaries and/or other parts of the flower following pollen germination.HighlightTolerance to heat stress was found not to confer tolerance to a combination of water deficit and heat stress in soybean, highlighting the need for breeding strategies targeting the stress combination.

Reactive oxygen species (ROS) are key signalling molecules that enable cells to rapidly respond to different stimuli. In plants, ROS play a crucial role in abiotic and biotic stress sensing, integration of different environmental signals and activation of stress-response networks, thus contributing to the establishment of defence mechanisms and plant resilience. Recent advances in the study of ROS signalling in plants include the identification of ROS receptors and key regulatory hubs that connect ROS signalling with other important stress-response signal transduction pathways and hormones, as well as new roles for ROS in organelle-to-organelle and cell-to-cell signalling. Our understanding of how ROS are regulated in cells by balancing production, scavenging and transport has also increased. In this Review, we discuss these promising developments and how they might be used to increase plant resilience to environmental stress.

Plants can send long-distance cell-to-cell signals from a single tissue subjected to stress to the entire plant. This ability is termed “systemic signaling” and is essential for plant acclimation to stress and/or defense against pathogens. Several signaling mechanisms are associated with systemic signaling, including the reactive oxygen species (ROS) wave, calcium wave, hydraulic wave, and electric signals. The ROS wave coordinates multiple physiological, molecular, and metabolic responses among different parts of the plant and is essential for systemic acquired acclimation (SAA) to stress. In addition, it is linked with several plant hormones, including jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). However, how these plant hormones modulate the ROS wave and whether they are required for SAA is not clear. Here we report that SA and JA play antagonistic roles in modulating the ROS wave in Arabidopsis (Arabidopsis thaliana). While SA augments the ROS wave, JA suppresses it during responses to local wounding or high light (HL) stress treatments. We further show that ethylene and ABA are essential for regulation of the ROS wave during systemic responses to local wounding treatment. Interestingly, we found that the redox-response protein NONEXPRESSOR OF PATHOGENESIS RELATED PROTEIN 1 is required for systemic ROS accumulation in response to wounding or HL stress, as well as for SAA to HL stress. Taken together, our findings suggest that interplay between JA and SA might regulate systemic signaling and SAA during responses of plants to abiotic stress or wounding.

Plants can send long distance cell-to-cell signals from a single tissue subjected to stress to the entire plant. This ability is termed ‘systemic signaling’ and is essential for plant acclimation to stress and/or defense against pathogens. Several signaling mechanisms are associated with systemic signaling, including the reactive oxygen species (ROS) wave, calcium wave, hydraulic wave, and electric signals. The ROS wave coordinates multiple physiological, molecular, and metabolic responses among different parts of the plant, and is essential for systemic acquired acclimation (SAA) to stress. In addition, it is linked with several plants hormones, including jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). However, how these plant hormones modulate the ROS wave and whether they are required for SAA is not clear. Here we report that SA and JA play antagonistic roles in modulating the ROS wave. While SA augments the ROS wave, JA suppresses it, during responses to a local wounding or high light (HL) stress treatments. We further show that ethylene and ABA are essential for the regulation of the ROS wave during systemic responses to a local wounding treatment. Interestingly, we found that the redox-response protein NONEXPRESSOR OF PATHOGENESIS RELATED PROTEIN 1 (NPR1) is required for systemic ROS accumulation in response to wounding or HL stress, as well as for SAA to HL stress. Taken together, our findings suggests that an interplay between JA and SA could regulate systemic signaling and SAA during responses of plants to abiotic stress or wounding.One sentence summaryAn antagonistic interaction between SA and JA attenuates the accumulation of ROS in local and systemic tissues during responses of plants to light stress or wounding.

Mechanical wounding occurs in plants during biotic (e.g., herbivore or pathogen attack) or abiotic (e.g., wind damage or freezing) stresses and is associated with the activation of multiple signaling pathways. These initiate many wound responses at the wounded tissues, as well as trigger long-distance signaling pathways that activate wound responses in tissues that were not affected by the initial wounding event (termed ‘systemic wound response’). Among the different systemic signals activated by wounding are electric signals, calcium and reactive oxygen species (ROS) waves, and different plant hormones such as jasmonic acid. The release of glutamate from cells at the wounded tissues was recently proposed to trigger several different systemic signal transduction pathways via glutamate-like receptors (GLRs). However, the role of another important compound released from cells during wounding (i.e., extracellular ATP; eATP) in triggering systemic responses is not clear. Here we show that eATP that accumulates in wounded leaves and is sensed by the purinoreceptor kinase P2K is required for the activation of the ROS wave during wounding. Application of eATP to unwounded leaves triggered the ROS wave, and the activation of the ROS wave by wounding or eATP application was suppressed in mutants deficient in P2K (i.e., p2k1-3, p2k2, and p2k1-3p2k2). In addition, the expression of several systemic wound response transcripts was suppressed in mutants deficient in P2K during wounding. Our findings reveal that in addition to sensing glutamate via GLRs, eATP sensed by P2Ks is playing a key role in the triggering of systemic wound responses in plants.One sentence summaryExtracellular ATP plays an important role in triggering the ROS wave and systemic transcriptomics responses during wounding.

As multicellular organisms, plants constantly balance and coordinate many metabolic, physiological, and molecular responses between different cell types and tissues. This process is essential for plant development, growth, and response to different environmental cues. Because plants lack a nervous system, they transmit different signals over long distances via cell-to-cell signaling. Recent studies revealed that reactive oxygen species (ROS), produced by respiratory burst oxidase homologs (RBOHs) at the apoplast play a key role in cell-to-cell signaling. A state of enhanced ROS production by one cell is thereby sensed by a neighboring cell, causing it to produce ROS, creating a continuous chain of cell-to-cell ROS accumulation termed the ‘ROS wave’. This process was found to mediate systemic signals throughout the plant and is required for plant acclimation to different stresses. Although RBOHs were found to produce ROS essential for this process, the identity of the receptor(s) perceiving the apoplastic ROS signal is currently unknow. Here we reveal that the leucine-rich-repeat receptor-like kinase HPCA1 (H2O2-induced Ca2+increases 1) acts as a central ROS receptor required for the propagation of cell-to-cell ROS signals, systemic signaling in response to different biotic and abiotic stresses, and plant acclimation to stress. We further report that HPCA1 is required for systemic calcium signals, but not systemic membrane depolarization responses, and identify key calcium-dependent signal transduction proteins involved in this process. Our findings reveal that HPCA1 plays a key role in mediating and coordinating systemic cell-to-cell ROS and calcium signals that are required for plant acclimation to stress.

Systemic signaling and systemic acquired acclimation (SAA) are essential for plant survival during episodes of environmental stress. Recent studies highlighted a key role for reactive oxygen species (ROS) signaling in mediating systemic responses and SAA during light stress in Arabidopsis (Arabidopsis thaliana). These studies further identified the RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) protein as a key player in mediating rapid systemic ROS responses. Here, we report that tissue-specific expression of RBOHD in phloem or xylem parenchyma cells of the rbohD mutant restores systemic ROS signaling, systemic stress-response transcript expression, and SAA to a local treatment of light stress. We further demonstrate that RBOHD and RBOHF are both required for local and systemic ROS signaling at the vascular bundles of Arabidopsis. Taken together, our findings highlight a key role for RBOHD-driven ROS production at the vascular bundles of Arabidopsis in mediating light stress–induced systemic signaling and SAA. In addition, they suggest that the integration of ROS, calcium, electric, and hydraulic signals, during systemic signaling, occurs at the vascular bundles.

Systemic acquired acclimation (SAA) is a key biological process essential for plant survival under conditions of abiotic stress. SAA was recently shown to be controlled by a rapid systemic signaling mechanism termed the reactive oxygen species (ROS) wave in Arabidopsis (Arabidopsis thaliana). MYB30 is a key transcriptional regulator mediating many different biological processes. MYB30 was found to act downstream of the ROS wave in systemic tissues of Arabidopsis in response to local high light (HL) stress treatment. However, the function of MYB30 in systemic signaling and SAA is unknown. To determine the relationship among MYB30, the ROS wave, and systemic acclimation in Arabidopsis, the SAA response to HL stress of myb30 mutants and wild-type plants was determined. Although myb30 plants were found to display enhanced rates of ROS wave propagation and their local tissues acclimated to the HL stress, they were deficient in SAA to HL stress. Compared to wild type, the systemic transcriptomic response of myb30 plants was also deficient, lacking in the expression of over 3,500 transcripts. A putative set of 150 core transcripts directly associated with MYB30 function during HL stress was determined. Our study identifies MYB30 as a key regulator that links systemic ROS signaling with systemic transcriptomic responses, SAA, and plant acclimation to HL stress. In addition, it demonstrates that plant acclimation and systemic ROS signaling are interlinked and that the lack of systemic acclimation drives systemic ROS signaling to occur at faster rates, suggesting a feedback mechanism (potentially involving MYB30) between these two processes.

Significance Environmental stresses such as heat, drought, and salinity, especially in combination with intense light conditions, can have devastating economical and sociological impacts. Although our knowledge of how each of these stresses affects plants when applied individually is vast, we know very little about how plants acclimate to a combination of different stresses. Here we reveal that plants can integrate different local and systemic signals generated during conditions of stress combination. We further show that the specific part at which plants sense the two co-occurring stresses makes a significant difference in how fast and efficient they acclimate. Our results shed light on how plants acclimate to and survive a combination of different stresses., Extreme environmental conditions, such as heat, salinity, and decreased water availability, can have a devastating impact on plant growth and productivity, potentially resulting in the collapse of entire ecosystems. Stress-induced systemic signaling and systemic acquired acclimation play canonical roles in plant survival during episodes of environmental stress. Recent studies revealed that in response to a single abiotic stress, applied to a single leaf, plants mount a comprehensive stress-specific systemic response that includes the accumulation of many different stress-specific transcripts and metabolites, as well as a coordinated stress-specific whole-plant stomatal response. However, in nature plants are routinely subjected to a combination of two or more different abiotic stresses, each potentially triggering its own stress-specific systemic response, highlighting a new fundamental question in plant biology: are plants capable of integrating two different systemic signals simultaneously generated during conditions of stress combination? Here we show that plants can integrate two different systemic signals simultaneously generated during stress combination, and that the manner in which plants sense the different stresses that trigger these signals (i.e., at the same or different parts of the plant) makes a significant difference in how fast and efficient they induce systemic reactive oxygen species (ROS) signals; transcriptomic, hormonal, and stomatal responses; as well as plant acclimation. Our results shed light on how plants acclimate to their environment and survive a combination of different abiotic stresses. In addition, they highlight a key role for systemic ROS signals in coordinating the response of different leaves to stress.

Reactive oxygen species (ROS) are key signalling molecules that enable cells to rapidly respond to different stimuli. In plants, ROS play a crucial role in abiotic and biotic stress sensing, integration of different environmental signals and activation of stress-response networks, thus contributing to the establishment of defence mechanisms and plant resilience. Recent advances in the study of ROS signalling in plants include the identification of ROS receptors and key regulatory hubs that connect ROS signalling with other important stress-response signal transduction pathways and hormones, as well as new roles for ROS in organelle-to-organelle and cell-to-cell signalling. Our understanding of how ROS are regulated in cells by balancing production, scavenging and transport has also increased. In this Review, we discuss these promising developments and how they might be used to increase plant resilience to environmental stress.

Heat waves, occurring during droughts, can have a devastating impact on yield, especially if they happen during the flowering and seed set stages of the crop cycle. Global warming and climate change are driving an alarming increase in the frequency and intensity of combined drought and heat stress episodes, critically threatening global food security. Previous studies revealed that during a combination of drought and heat stress stomata on leaves of many plants are closed, preventing cooling by transpiration. Because high temperature is detrimental to reproductive processes, essential for plant yield, we measured the inner temperature, transpiration, and sepal stomatal aperture of closed soybean flowers, developing on plants subjected to a combination of drought and heat stress. Here, we report that during a combination of drought and heat stress soybean plants prioritize transpiration through flowers over transpiration through leaves by opening their flower stomata, while keeping their leaf stomata closed. This acclimation strategy, termed ‘differential transpiration’, lowers flower inner temperature by about 2-3°C, protecting reproductive processes at the expense of vegetative tissues. Manipulating stomatal regulation, stomatal size and/or stomatal density of flowers could therefore serve as a viable strategy to enhance the yield of different crops and mitigate some of the current and future impacts of global warming and climate change on agriculture.One sentence summaryDuring stress conditions that result in higher flower inner temperature plants use a differential transpiration strategy to protect reproductive processes at the expense of vegetative tissues.

Background Therapy with mesenchymal stem cells remains a promising but challenging approach to critical limb ischemia in diabetes because of the dismal cell survival. Methods and Results Critical limb ischemia in type 2 diabetes mouse model was used to explore the impact of diabetic limb ischemia on the survival of bone marrow mesenchymal stromal cells (bMSCs). Inhibition of intracellular reactive oxygen species was achieved with concomitant overexpression of superoxide dismutase (SOD)‐1 and glutathione peroxidase‐1 in the transplanted bMSCs, and extracellular reactive oxygen species was attenuated using SOD‐3 overexpression and N‐acetylcysteine treatment. In vivo optical fluorescence imaging and laser Doppler perfusion imaging were used to track cell retention and determine blood flow in diabetic ischemic limb, respectively. Survival of the transplanted bMSCs was significantly decreased in diabetic ischemic limb compared with the control. In vitro study indicated that advanced glycation end products, not high glucose, significantly decreased the proliferation of bMSCs and increased their apoptosis associated with increased reactive oxygen species production and selective reduction of SOD‐1 and SOD‐3. In vivo study demonstrated that concomitant overexpression of SOD‐1, SOD‐3, and glutathione peroxidase‐1, or host treatment with N‐acetylcysteine, significantly enhanced in vivo survival of transplanted bMSCs, and improved critical limb ischemia in diabetic mice. Combination of triple antioxidant enzyme overexpression in bMSCs with host N‐acetylcysteine treatment further improved bMSC survival with enhanced circulatory and functional recovery from diabetic critical limb ischemia. Conclusions Simultaneous suppression of reactive oxygen species from transplanted bMSCs and host tissue could additively enhance bMSC survival in diabetic ischemic limb with increased therapeutic efficacy in diabetes.

Plants are essential for life on Earth converting light into chemical energy in the form of sugars. To adjust for changes in light intensity and quality, and to become as efficient as possible in harnessing light, plants utilize multiple light receptors, signaling, and acclimation mechanisms. In addition to altering plant metabolism, development and growth, light cues sensed by some photoreceptors, such as phytochromes, impact on many plant responses to biotic and abiotic stresses. Central for plant responses to different stresses are reactive oxygen species (ROS) that function as key signaling molecules. Recent studies demonstrated that respiratory burst oxidase homolog (RBOH) proteins that reside at the plasma membrane and produce ROS at the apoplast play a key role in plant responses to different biotic and abiotic stresses. Here we reveal that phytochrome B (phyB) and RBOHs function as part of a key regulatory module that controls ROS production, transcript expression, and plant acclimation to excess light stress. We further show that phyB can regulate ROS production during stress even if it is restricted to the cytosol, and that phyB, RBOHD and RBOHF co-regulate thousands of transcripts in response to light stress. Surprisingly, we found that phyB is also required for ROS accumulation in response to heat, wounding, cold, and bacterial infection. Taken together, our findings reveal that phyB plays a canonical role in plant responses to biotic and abiotic stresses, regulating ROS production, and that phyB and RBOHs function in the same pathway.Significant StatementAbiotic and biotic stresses cause extensive losses to agricultural production and threaten global food security. Augmenting plant resilience to stressful conditions requires understanding of how plants sense stress. Here we report that the sensing of different abiotic and biotic stresses that result in the production of the key stress-response signaling molecules, reactive oxygen species, requires the plant photoreceptor protein phytochrome B. We further show that in contrast to its many nuclear functions, phytochrome B regulates reactive oxygen production by plasma membrane-localized respiratory burst oxidase homologs while localized to the cytosol. Our findings reveal the existence of a rapid stress response regulatory mechanism requiring phytochrome B and reactive oxygen species, essential for plant acclimation to stress.

The sensing of abiotic stress, mechanical injury, or pathogen attack by a single plant tissue results in the activation of systemic signals that travel from the affected tissue to the entire plant, alerting it of an impending stress or pathogen attack. This process is essential for plant survival during stress and is termed systemic signaling. Among the different signals triggered during this process are calcium, electric, reactive oxygen species (ROS) and hydraulic signals. These are thought to propagate at rapid rates through the plant vascular bundles and to regulate many of the systemic processes essential for plant survival. Although the different signals activated during systemic signaling are thought to be interlinked, their coordination and hierarchy remain to be determined. Here, using a combination of advanced whole-plant imaging and hydraulic pressure measurements, we studied the activation of all four systemic signals in wild type and different Arabidopsis thaliana mutants subjected to a local high light (HL) stress or wounding. Our findings reveal that in response to wounding systemic changes in membrane potential, calcium, ROS, and hydraulic pressure are coordinated by glutamate receptor-like (GLR) proteins 3.3 and 3.6, while in response to HL the respiratory burst oxidase homolog D-driven systemic ROS signal could be separated from systemic changes in membrane potential and calcium levels. We further determine that plasmodesmata functions are required for systemic changes in membrane potential, calcium, and ROS during systemic signaling. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress.Significance statementThe ability of plants to transmit a signal from a stressed or wounded tissue to the entire plant, termed systemic signaling, is key to plant survival during conditions of environmental stress. At least four different systemic signals are thought to be involved in this process: electric, calcium, reactive oxygen and hydraulic. However, how are they coordinated and whether they can be stress-specific is mostly unknown. Here we report that different types of stimuli can induce different types of systemic signals that may or may not be linked with each other. We further reveal that hydraulic waves can be actively regulated in plants in response to wounding, and that proteins that regulate plasmodesmata pores play a key role in systemic signaling.

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (the local tissue) to the entire plant (systemic tissues). Reactive oxygen species (ROS) and Ca

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (the local tissue) to the entire plant (systemic tissues). Reactive oxygen species (ROS) and Ca2+ are key signaling molecules thought to be involved in this cell-to-cell mechanism. Here, we report that the systemic response of Arabidopsis thaliana to a local treatment of high light stress, which resulted in local ROS accumulation, required ROS generated by respiratory burst oxidase homolog D (RBOHD). ROS increased cell-to-cell transport and plasmodesmata (PD) pore size in a manner dependent on PD-localized protein 1 (PDLP1) and PDLP5, and this process was required for the propagation of the systemic ROS signals and SAA. Furthermore, aquaporins and several Ca2+-permeable channels in the glutamate receptor-like (GLR), mechanosensitive small conductance-like (MSL), and cyclic nucleotide-gated (CNGC) families were involved in this systemic signaling process. However, we determined that these channels were required primarily to amplify the systemic signal in each cell along the path of the systemic ROS wave, as well as to establish local and systemic acclimation. Thus, PD and RBOHD-generated ROS orchestrate light stress-induced rapid cell-to-cell spread of systemic signals in Arabidopsis.

Reactive oxygen species (ROS) play a key role in regulating plant responses to different abiotic stresses, wounding and pathogen attack. In addition to triggering responses at the tissues directly subjected to stress, ROS were recently shown to mediate a rapid whole-plant systemic signal, termed the “ROS wave”, required for inducing a state of systemic acquired acclimation, or systemic wound response. However, whether the ROS wave that spreads from the local tissues subjected to wounding to the rest of the plant triggers alterations in redox levels, is mostly unknown at present. Here, using a genetically-encoded reporter for cellular glutathione redox changes, roGFP1, we show that the wounding-induced systemic ROS wave in Arabidopsis thaliana is accompanied by a rapid systemic wave of cytosolic redox oxidation, termed a “redox wave”. The ROS wave may therefore trigger changes in redox levels in systemic leaves that in turn can trigger transcriptional, metabolic and proteomic changes resulting in acclimation and/or systemic wound responses.One sentence summaryThe wounding-induced reactive oxygen species (ROS) wave is accompanied by a systemic whole-plant redox response.

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (local tissue) to the entire plant (systemic tissues). Among the different systemic signaling molecules and processes thought to be involved in this cell-to-cell signaling mechanism are reactive oxygen species (ROS), calcium, electric and hydraulic signals. How these different signals and processes are interlinked, and how they transmit the systemic signal all the way from the local tissue to the entire plant, remain however largely unknown. Here, studying the systemic response of Arabidopsis thaliana to a local treatment of excess light stress, we report that respiratory burst oxidase homolog D (RBOHD)-generated ROS enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of systemic signals during responses to light stress. We further identify aquaporins, and several different calcium-permeable channels, belonging to the glutamate receptor-like, mechanosensitive small conductance-like, and cyclic nucleotide-gated families, as involved in this process, but determine that their function is primarily required for the maintenance of the signal in each cell along the path of the systemic signal, as well as for the establishment of acclimation at the local and systemic tissues. PD and RBOHD-generated ROS orchestrate therefore light stress-induced rapid cell-to-cell spread of systemic signals in Arabidopsis.One-sentence summaryRespiratory burst oxidase homolog D-generated reactive oxygen species enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of the PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of rapid systemic signals during the response of Arabidopsis to excess light stress.

Because of their sessile nature, plants evolved integrated defense and acclimation mechanisms to simultaneously cope with adverse biotic and abiotic conditions. Among these are systemic acquired resistance (SAR) and systemic acquired acclimation (SAA). Growing evidence suggests that SAR and SAA activate similar cellular mechanisms and employ common signaling pathways for the induction of acclimatory and defense responses. It is therefore possible to consider these processes together, rather than separately, as a common systemic acquired acclimation and resistance (SAAR) mechanism.Arabidopsis thaliana flavin-dependent monooxygenase 1 (FMO1) was previously described as a regulator of plant resistance in response to pathogens as an important component of SAR. In the current study, we investigated its role in SAA, induced by a partial exposure of Arabidopsis rosette to local excess light stress. We demonstrate here that FMO1 expression is induced in leaves directly exposed to excess light stress as well as in systemic leaves remaining in low light. We also show that FMO1 is required for the systemic induction of ASCORBATE PEROXIDASE 2 (APX2) and ZINC-FINGER OF ARABIDOPSIS 10 (ZAT10) expression and spread of the reactive oxygen species (ROS) systemic signal in response to a local application of excess light treatment. Additionally, our results demonstrate that FMO1 is involved in the regulation of excess light-triggered systemic cell death, which is under control of LESION SIMULATING DISEASE 1 (LSD1). Our study indicates therefore that FMO1 plays an important role in triggering SAA response, supporting the hypothesis that SAA and SAR are tightly connected and use the same signaling pathways.

Systemic signaling in plants is orchestrated by a complex network of interconnected systemic signals and cell types. In this issue of Science Signaling, Shao et al unveil how different wound-induced signals integrate into a well-regulated systemic response.

Each year, abiotic stress conditions such as drought, heat, salinity, cold and particularly their different combinations, inflict a heavy toll on crop productivity worldwide. The effects of these adverse conditions on plant productivity are becoming ever more alarming in recent years in light of the increased rate and intensity of global climatic changes. Improving crop tolerance to abiotic stress conditions requires a deep understanding of the response of plants to changes in their environment. This response is dependent on early and late signal transduction events that involve important signaling molecules such as reactive oxygen species (ROS), different plant hormones and other signaling molecules. It is the integration of these signaling events, mediated by an interplay between ROS and different plant hormones that orchestrates the plant response to abiotic stress and drive changes in transcriptomic, metabolic and proteomic networks that lead to plant acclimation and survival. Here we review some of the different studies that address hormone and ROS integration during the response of plants to abiotic stress. We further highlight the integration of ROS and hormone signaling during early and late phases of the plant response to abiotic stress, the key role of respiratory burst oxidase homologs in the integration of ROS and hormone signaling during these phases, and the involvement of hormone and ROS in systemic signaling events that lead to systemic acquired acclimation. Lastly, we underscore the need to understand the complex interactions that occur between ROS and different plant hormones during stress combinations.

Rapidly communicating the perception of an abiotic stress event, wounding or pathogen infection, from its initial site of occurrence to the entire plant, i.e. rapid systemic signaling, is essential for successful plant acclimation and defense. Recent studies highlighted an important role for several rapid whole-plant systemic signals in mediating plant acclimation and defense during different abiotic and biotic stresses. These include calcium, reactive oxygen species (ROS), hydraulic and electric waves. Although the role of some of these signals in inducing and coordinating whole-plant systemic responses was demonstrated, many questions related to their mode of action, routes of propagation and integration remain unanswered. In addition, it is unclear how these signals convey specificity to the systemic response, and how are they integrated under conditions of stress combination. Here we highlight many of these questions, as well as provide a proposed model for systemic signal integration, focusing on the ROS wave.

Reactive oxygen species (ROS) are key regulators of numerous subcellular, cellular, and systemic signals. They function in plants as an integral part of many different hormonal, physiological, and developmental pathways, as well as play a critical role in defense and acclimation responses to different biotic and abiotic conditions. Although many ROS imaging techniques have been developed and utilized in plants, a whole-plant imaging platform for the dynamic detection of ROS in mature plants is lacking. Here we report a robust and straightforward method for the whole-plant live imaging of ROS in mature plants grown in soil. This new method could be used to study local and systemic ROS signals in different genetic variants, conduct phenotyping studies to identify new pathways for ROS signaling, monitor the stress level of different plants and mutants, and unravel novel routes of ROS integration into stress, growth regulation, and development in plants. We demonstrate the utility of this new method for studying systemic ROS signals in different Arabidopsis mutants and wound responses in cereals such as wheat and corn.

Water is a key factor in plant life. Therefore, reaching and holding water is a crucial part in plant survival. Plants sense water through a set of sensors which includes sensors for water activity (potential), for specific components of water potential, or for specific solutes contributing to water potential and for hydraulic signals. While these sensors are common to different plants and other organisms, their functions and modes of action are yet far from being understood. It is also unknown how these sensing mechanisms are linked to cellular and whole-plant responses to changes in water status in the soil or in the atmosphere. Advanced technologies that would provide means for single-cell physiological manipulations together with high-throughput noninvasive real-time monitoring systems of shoots and roots and advanced biochemistry and structural studies at atomic resolution of sensor proteins and protein complexes are imperative for understanding water sensing by plants.

Proline is not only an essential component of proteins but it also has important roles in adaptation to osmotic and dehydration stresses, redox control, and apoptosis. Here, we review pathways of proline biosynthesis in the three domains of life. Pathway reconstruction from genome data for hundreds of eubacterial and dozens of archaeal and eukaryotic organisms revealed evolutionary conservation and variations of this pathway across different taxa. In the most prevalent pathway of proline synthesis, glutamate is phosphorylated to γ-glutamyl phosphate by γ-glutamyl kinase, reduced to γ-glutamyl semialdehyde by γ-glutamyl phosphate reductase, cyclized spontaneously to Δ(1)-pyrroline-5-carboxylate and reduced to proline by Δ(1)-pyrroline-5-carboxylate reductase. In higher plants and animals the first two steps are catalysed by a bi-functional Δ(1) -pyrroline-5-carboxylate synthase. Alternative pathways of proline formation use the initial steps of the arginine biosynthetic pathway to ornithine, which can be converted to Δ(1)-pyrroline-5-carboxylate by ornithine aminotransferase and then reduced to proline or converted directly to proline by ornithine cyclodeaminase. In some organisms, the latter pathways contribute to or could be fully responsible for the synthesis of proline. The conservation of proline biosynthetic enzymes and significance of specific residues for catalytic activity and allosteric regulation are analysed on the basis of protein structural data, multiple sequence alignments, and mutant studies, providing novel insights into proline biosynthesis in organisms. We also discuss the transcriptional control of the proline biosynthetic genes in bacteria and plants.

Proline is not only an essential component of proteins but it also has important roles in adaptation to osmotic and dehydration stresses, redox control, and apoptosis. Here, we review pathways of proline biosynthesis in the three domains of life. Pathway reconstruction from genome data for hundreds of eubacterial and dozens of archaeal and eukaryotic organisms revealed evolutionary conservation and variations of this pathway across different taxa. In the most prevalent pathway of proline synthesis, glutamate is phosphorylated to γ-glutamyl phosphate by γ-glutamyl kinase, reduced to γ-glutamyl semialdehyde by γ-glutamyl phosphate reductase, cyclized spontaneously to Δ(1)-pyrroline-5-carboxylate and reduced to proline by Δ(1)-pyrroline-5-carboxylate reductase. In higher plants and animals the first two steps are catalysed by a bi-functional Δ(1) -pyrroline-5-carboxylate synthase. Alternative pathways of proline formation use the initial steps of the arginine biosynthetic pathway to ornithine, which can be converted to Δ(1)-pyrroline-5-carboxylate by ornithine aminotransferase and then reduced to proline or converted directly to proline by ornithine cyclodeaminase. In some organisms, the latter pathways contribute to or could be fully responsible for the synthesis of proline. The conservation of proline biosynthetic enzymes and significance of specific residues for catalytic activity and allosteric regulation are analysed on the basis of protein structural data, multiple sequence alignments, and mutant studies, providing novel insights into proline biosynthesis in organisms. We also discuss the transcriptional control of the proline biosynthetic genes in bacteria and plants.