Summary
Human activity is causing a global change in plant environment that includes a significant increase in the number and intensity of different stress factors. These include combinations of ...multiple abiotic and biotic stressors that simultaneously or sequentially impact plants and microbiomes, causing a significant decrease in plant growth, yield and overall health. It was recently found that with the increasing number and complexity of stressors simultaneously impacting a plant, plant growth and survival decline dramatically, even if the level of each individual stress, involved in such ‘multifactorial stress combination’, is low enough not to have a significant effect. Here we highlight this new concept of multifactorial stress combination and discuss its importance for our efforts to develop climate change‐resilient crops.
Global warming, climate change, and environmental pollution present plants with unique combinations of different abiotic and biotic stresses. Although much is known about how plants acclimate to each ...of these individual stresses, little is known about how they respond to a combination of many of these stress factors occurring together, namely a multifactorial stress combination. Recent studies revealed that increasing the number of different co-occurring multifactorial stress factors causes a severe decline in plant growth and survival, as well as in the microbiome biodiversity that plants depend upon. This effect should serve as a dire warning to our society and prompt us to decisively act to reduce pollutants, fight global warming, and augment the tolerance of crops to multifactorial stress combinations.
A multifactorial stress combination occurs when more than two to three abiotic and/or biotic stress factors simultaneously impact a plant.Global warming, climate change, and industrial pollution could result in an increase in the frequency, complexity, and intensity of multifactorial stress combinations impacting plants, soils, and microbial communities.With the increase in the number of factors simultaneously impacting plants, the survival and growth of plants declines, even if the levels of each of these individual stresses is very low.The response of plants to a multifactorial stress combination is unique and involves many transcripts and genes that are not altered in response to each of the different stresses applied individually.The harmful effects of a multifactorial stress combination on the survival and growth of plants, different soil properties, and diversity of microbial communities should serve as a dire warning to our society and prompt us to act drastically to reduce the different sources of multifactorial stresses in our environment.
SUMMARY
Global warming and climate change are driving an alarming increase in the frequency and intensity of different abiotic stresses, such as droughts, heat waves, cold snaps, and flooding, ...negatively affecting crop yields and causing food shortages. Climate change is also altering the composition and behavior of different insect and pathogen populations adding to yield losses worldwide. Additional constraints to agriculture are caused by the increasing amounts of human‐generated pollutants, as well as the negative impact of climate change on soil microbiomes. Although in the laboratory, we are trained to study the impact of individual stress conditions on plants, in the field many stresses, pollutants, and pests could simultaneously or sequentially affect plants, causing conditions of stress combination. Because climate change is expected to increase the frequency and intensity of such stress combination events (e.g., heat waves combined with drought, flooding, or other abiotic stresses, pollutants, and/or pathogens), a concentrated effort is needed to study how stress combination is affecting crops. This need is particularly critical, as many studies have shown that the response of plants to stress combination is unique and cannot be predicted from simply studying each of the different stresses that are part of the stress combination. Strategies to enhance crop tolerance to a particular stress may therefore fail to enhance tolerance to this specific stress, when combined with other factors. Here we review recent studies of stress combinations in different plants and propose new approaches and avenues for the development of stress combination‐ and climate change‐resilient crops.
Significance Statement
Climate change and global warming increase the likelihood that trees and crop plants will be subjected to a combination of different abiotic and biotic stresses, compromising global food production and security. This paper reviews recent advances in the study of plant responses to stress combinations and proposes potential strategies to develop crops with high resilience to a wide range of stress factors and their combination.
Summary
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.
Significance Statement
Reactive oxygen species and plant hormones play a key role in coordinating the response of plants to different abiotic stresses, as well as in inducing a state of heightened acclimation to different abiotic stress conditions. Here we review some of the vast recent and early literature describing how reactive oxygen species and hormonal signaling are integrated during abiotic stress, stress combinations and systemic signaling.
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.
Reactive oxygen species (ROS), produced by respiratory burst oxidase homologs (RBOHs) at the apoplast, play a key role in local and systemic cell-to-cell signaling, required for plant acclimation to ...stress. Here we reveal that the Arabidopsis thaliana leucine-rich-repeat receptor-like kinase H2O2-INDUCED CA2+ INCREASES 1 (HPCA1) 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, stress responses at the local and systemic tissues, and plant acclimation to stress, following a local treatment of high light (HL) stress. We further report that HPCA1 is required for systemic calcium signals, but not systemic membrane depolarization responses, and identify the calcium-permeable channel MECHANOSENSITIVE ION CHANNEL LIKE 3, CALCINEURIN B-LIKE CALCIUM SENSOR 4 (CBL4), CBL4-INTERACTING PROTEIN KINASE 26 and Sucrose-non-fermenting-1-related Protein Kinase 2.6/OPEN STOMATA 1 (OST1) as required for the propagation of cell-to-cell ROS signals. In addition, we identify serine residues S343 and S347 of RBOHD (the putative targets of OST1) as playing a key role in cell-to-cell ROS signaling in response to a local application of HL stress. Our findings reveal that HPCA1 plays a key role in mediating and coordinating systemic cell-to-cell ROS and calcium signals required for plant acclimation to stress.
Reactive oxygen species (ROS) play a key signaling role in plant and animal cells. Among the many cellular mechanisms used to generate and transduce ROS signals, ROS-induced ROS release (RIRR) is ...emerging as an important pathway involved in different human pathologies and plant responses to environmental stress. RIRR is a process in which one cellular compartment or organelle generates or releases ROS, triggering the enhanced production or release of ROS by another compartment or organelle. It was initially described in animal cells and proposed to mediate mitochondria-to-mitochondria communication, but later expanded to include communication between mitochondria and plasma membrane-localized NADPH oxidases. In plants a process of RIRR was demonstrated to mediate long distance rapid systemic signaling in response to biotic and abiotic stress. This process is thought to involve the enhanced production of ROS by one cell that triggers the enhanced production of ROS by a neighboring cell in a process that propagates the enhanced “ROS production state” all the way from one part of the plant to another. In contrast to the intracellular nature of the RIRR process of animal cells, the plant RIRR process is therefore primarily studied at the cell-to-cell communication level. Studies on intracellular (organelle-to-organelle, or organelle-to-NADPH oxidase) RIRR pathways are very scarce in plants, whereas studies on cell-to-cell RIRR are very scarce in animals. Here we will attempt to highlight what is known in both systems and what each system can learn from the other.
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•ROS-induced ROS release (RIRR) plays a key signaling role in plant and animal cells.•In plants RIRR mediates cell-to-cell communication.•In animals RIRR mediates intracellular communication.•Could RIRR pathways mediate intercellular signaling in animals?•Could RIRR pathways mediate intracellular signaling in plants?
Climate change is predicted to increase the frequency and intensity of abiotic stress combinations that negatively impact plants and pose a serious threat to crop yield and food supply. Plants ...respond to episodes of stress combination by activating specific physiological and molecular responses, as well as by adjusting different metabolic pathways, to mitigate the negative effects of the stress combination on plant growth, development, and reproduction. Plants synthesize a wide range of metabolites that regulate many aspects of plant growth and development, as well as plant responses to stress. Although metabolic responses to individual abiotic stresses have been studied extensively in different plant species, recent efforts have been directed at understanding metabolic responses that occur when different abiotic factors are combined. In this review we examine recent studies of metabolomic changes under stress combination in different plants and suggest new avenues for the development of stress combination-resilient crops based on metabolites as breeding targets.
Under field conditions crops are routinely subjected to a number of different abiotic stress factors simultaneously. Recent studies revealed that the response of plants to a combination of different ...abiotic stresses is unique and cannot be directly extrapolated from simply studying each of the different stresses applied individually. These studies have also identified specific regulatory transcripts, combinations of metabolites and proteins, and physiological responses that are unique to specific stress combinations, highlighting the importance of studying abiotic stress combination in plants. Here we describe the interactions between drought and other abiotic stresses with emphasis on drought and heat stress. We compile new data about the different molecular, physiological and metabolic adaptations of different plants and crops to this stress combination and we highlight the importance of reactive oxygen species (ROS) metabolism and stomatal responses for plant acclimation to drought and heat stress combination. We further emphasize the need for developing crops with enhanced tolerance to drought and heat stress combination in order to mitigate the negative impacts of predicted global climatic changes on agricultural production worldwide.
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