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.

Plants grow and reproduce within a highly dynamic environment that can see abrupt changes in conditions, such as light intensity, temperature, humidity, or interactions with biotic agents. Recent studies revealed that plants can respond within seconds to some of these conditions, engaging many different metabolic and molecular networks, as well as rapidly altering their stomatal aperture. Some of these rapid responses were further shown to propagate throughout the entire plant via waves of reactive oxygen species (ROS) and Ca 2+ that are possibly mediated through the plant vascular system. Here, we propose that the integration of these signals is mediated through pulses of gene expression that are coordinated throughout the plant in a systemic manner by the ROS/Ca +2 waves. The Dynamic Environment of PlantsWhile growing within their natural habitat, or in a manmade field environment, plants are subjected to many different changes in their physical and biological surroundings. These can be gradual, such as the slow decrease in soil water content over time during summer, or rapid, such as changes in light intensity occurring as a result of sun flecks during a cloudy day [1-9] (Figure 1, Key Figure). Some of these rapid changes can occur simultaneously, or on the background of other more persistent stress conditions, such as a prolonged drought or a heat wave, essentially representing a state of stress combination [4,5,10]. In addition, due to the placement of the plant within its environment, for example its position within a row of plants or plot in the field, or its position in nature in close proximity to a tree cover, not all parts or tissues of the plant may experience the rapid change in environmental conditions simultaneously [4,11]. Under such conditions, the rapid responses (see Glossary) at the affected tissue could trigger systemic signaling pathways, such as the ROS [12] and calcium waves [13], electric signals [14], and/or hydraulic waves [15]. The occurrence of rapid changes in the physical and/ or biological environment of the plant, coupled with the discovery of rapid systemic signaling pathways activated by many of these conditions [12][13][14][15], and the discovery of rapid transcriptional and metabolic responses to stress [16,17], support a hypothesis that plants evolved sensing and acclimation mechanisms that may function [ 3 9 0 _ T D $ D I F F ] within the seconds to minute timescale and are important for the overall fitness of the plant and its ability to survive rapid changes within its environment (Figure 1). Here, we examine the molecular networks, and physiological and metabolic changes that occur in plants during rapid responses to stress, and propose that the integration of these responses is mediated through pulses of gene expression that are coordinated throughout the plant in a systemic manner by [ 3 9 1 _ T D $ D I F F ] the ROS/Ca +2 waves. HighlightsRecent studies reveal that plants respond within the seconds to minutes time-scale to different biotic and/or abiotic stimuli.The ra...

R.M. wrote the article and prepared figures; all authors read and approved the final version of the article. [OPEN] Articles can be viewed without a subscription.

Climate change-driven extreme weather events, combined with increasing temperatures, harsh soil conditions, low water availability and quality, and the introduction of many manmade pollutants, pose a unique challenge to plants. Although our knowledge of the response of plants to each of these individual conditions is vast, we know very little about how a combination of many of these factors, occurring simultaneously, that is multifactorial stress combination, impacts plants. Seedlings of wild-type and different mutants of Arabidopsis thaliana plants were subjected to a multifactorial stress combination of six different stresses, each applied at a low level, and their survival, physiological and molecular responses determined. Our findings reveal that, while each of the different stresses, applied individually, had a negligible effect on plant growth and survival, the accumulated impact of multifactorial stress combination on plants was detrimental. We further show that the response of plants to multifactorial stress combination is unique and that specific pathways and processes play a critical role in the acclimation of plants to multifactorial stress combination. Taken together our findings reveal that further polluting our environment could result in higher complexities of multifactorial stress combinations that in turn could drive a critical decline in plant growth and survival.

These authors contributed equally. SUMMARYSystemic acquired acclimation (SAA) plays a key role in optimizing growth and preventing damage associated with fluctuating or abrupt changes in the plant environment. To be effective, SAA has to occur at a rapid rate and depend on rapid signaling pathways that transmit signals from affected tissues to all parts of the plant. Although recent studies have identified several different rapid systemic signaling pathways that could mediate SAA, very little information is known about the extent of their involvement in mediating transcriptomic responses. Here we reveal that the systemic transcriptomic response of plants to excess light stress is extensive in its context and involves an early (2 min) and transient stage of transcript expression that includes thousands of genes. This early response is dependent on the respiratory burst oxidase homolog D protein, and the function of the reactive oxygen species (ROS) wave. We further identify a core set of transcripts associated with the ROS wave and suggest that some of these transcripts are involved in linking ROS with calcium signaling. Priming of a systemic leaf to become acclimated to a particular stress during SAA involves thousands of transcripts that display a rapid and transient expression pattern driven by the ROS wave.