Summary
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.
Significance Statement
Systemic signaling pathways play a key role in the successful acclimation and defense of plants against different abiotic and biotic stresses.In this focused review we summarize recent studies addressing the different signals that mediate systemic signaling, as well as propose a model for their integration.
Farmers and breeders have long known that often it is the simultaneous occurrence of several abiotic stresses, rather than a particular stress condition, that is most lethal to crops. Surprisingly, ...the co-occurrence of different stresses is rarely addressed by molecular biologists that study plant acclimation. Recent studies have revealed that the response of plants to a combination of two different abiotic stresses is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Tolerance to a combination of different stress conditions, particularly those that mimic the field environment, should be the focus of future research programs aimed at developing transgenic crops and plants with enhanced tolerance to naturally occurring environmental conditions.
Systemic responses to environmental stimuli are essential for the survival of multicellular organisms. In plants, they are initiated in response to many different signals including pathogens, ...wounding, and abiotic stresses. Recent studies highlighted the importance of systemic acquired acclimation to abiotic stresses in plants and identified several different signals involved in this response. These included reactive oxygen species (ROS) and calcium waves, hydraulic waves, electric signals, and abscisic acid (ABA). Here, we address the interactions between ROS and ABA at the local and systemic tissues of plants subjected to abiotic stress and attempt to propose a model for the involvement of ROS, ABA, and stomata in systemic signaling leading to systemic acquired acclimation.
SUMMARY
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. 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 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 still need 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 treatment of high‐light (HL) stress or wounding. Our findings reveal that activation of systemic membrane potential, calcium, reactive oxygen species and hydraulic pressure signals, in response to wounding, is dependent on glutamate receptor‐like proteins 3.3 and 3.6. In contrast, in response to HL stress, systemic changes in calcium and membrane potential depended on glutamate receptor‐like 3.3 and 3.6, while systemic hydraulic signals did not. We further show that plasmodesmata functions are required for systemic changes in membrane potential and calcium during responses to HL stress or wounding. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress.
Significance Statement
At least four different signals are thought to mediate rapid systemic signaling in plants: electric, calcium, reactive oxygen species and hydraulic. Using newly developed whole‐plant imaging methods and hydraulic pressure probes, we studied the activation of all four signals in different Arabidopsis mutants subjected to local treatment of high light stress or wounding, revealing a key role for glutamate receptor‐like proteins in regulating hydraulic signals during systemic responses to wounding.
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
Reactive oxygen species (ROS) play a key role in the acclimation process of plants to abiotic stress. They primarily function as signal transduction molecules that regulate different pathways ...during plant acclimation to stress, but are also toxic byproducts of stress metabolism. Because each subcellular compartment in plants contains its own set of ROS‐producing and ROS‐scavenging pathways, the steady‐state level of ROS, as well as the redox state of each compartment, is different at any given time giving rise to a distinct signature of ROS levels at the different compartments of the cell. Here we review recent studies on the role of ROS in abiotic stress in plants, and propose that different abiotic stresses, such as drought, heat, salinity and high light, result in different ROS signatures that determine the specificity of the acclimation response and help tailor it to the exact stress the plant encounters. We further address the role of ROS in the acclimation of plants to stress combination as well as the role of ROS in mediating rapid systemic signaling during abiotic stress. We conclude that as long as cells maintain high enough energy reserves to detoxify ROS, ROS is beneficial to plants during abiotic stress enabling them to adjust their metabolism and mount a proper acclimation response.
Significance Statement
Reactive oxygen species (ROS) primarily function as signal transduction molecules that regulate different pathways during acclimation to stress, but are also toxic byproducts of stress metabolism. Different subcellular compartments contain different sets of ROS‐producing and ROS‐scavenging pathways, and thus ROS levels can have different signatures in different cellular compartments. Here we review recent work on ROS and abiotic stress, and propose that different stresses, such as drought, heat, salinity and high light, result in different ROS signatures that determine the specificity of the acclimation response to a particular stress.
Abiotic stress conditions such as drought, heat, or salinity cause extensive losses to agricultural production worldwide. Progress in generating transgenic crops with enhanced tolerance to abiotic ...stresses has nevertheless been slow. The complex field environment with its heterogenic conditions, abiotic stress combinations, and global climatic changes are but a few of the challenges facing modern agriculture. A combination of approaches will likely be needed to significantly improve the abiotic stress tolerance of crops in the field. These will include mechanistic understanding and subsequent utilization of stress response and stress acclimation networks, with careful attention to field growth conditions, extensive testing in the laboratory, greenhouse, and the field; the use of innovative approaches that take into consideration the genetic background and physiology of different crops; the use of enzymes and proteins from other organisms; and the integration of QTL mapping and other genetic and breeding tools.
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.
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