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.

Summary: Climate change‐driven extreme weather events, combined with increasing temperatures, harsh soil conditions, low water availability and quality, and the introduction of many man‐made 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.

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 Ca2+ 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.

In the field, plants experience high light (HL) intensities that are often accompanied by elevated temperatures. Such conditions are a serious threat to agriculture production, because photosynthesis is highly sensitive to both HL intensities and high-temperature stress. One of the potential cellular targets of HL and heat stress (HS) combination is PSII because its degree of photoinhibition depends on the balance between the rate of PSII damage (induced by light stress), and the rate of PSII repair (impaired under HS). Here, we studied the responses of Arabidopsis (Arabidopsis thaliana) plants to a combination of HL and HS (HL+HS) conditions. Combined HL+HS was accompanied by irreversible damage to PSII, decreased D1 (PsbA) protein levels, and an enhanced transcriptional response indicative of PSII repair activation. We further identified several unique aspects of this stress combination that included enhanced accumulation of jasmonic acid (JA) and JA-Ile, elevated expression of over 2,200 different transcripts that are unique to the stress combination (including many that are JA-associated), and distinctive structural changes to chloroplasts. A mutant deficient in JA biosynthesis (allene oxide synthase) displayed enhanced sensitivity to combined HL+HS and further analysis revealed that JA is required for regulating several transcriptional responses unique to the stress combination. Our study reveals that JA plays an important role in the acclimation of plants to a combination of HL+HS.

Reactive oxygen species (ROS) play a key role in the regulation of many biological processes in plants. Nonetheless, they are considered highly reactive and toxic to cells. Owing to their toxicity, as well as their important role in signaling, the level of ROS in cells needs to be tightly regulated. The ROS gene network, encoding a highly redundant arsenal of ROS scavenging mechanisms and an array of enzymes involved in ROS production, regulates ROS metabolism and signaling in plants. In this article, we review the role of the ROS gene network in plants and examine how it evolved. We identify key components of the ROS gene network in organisms that likely originated as early as 4.1–3.5 billion years ago, prior to the great oxidation event that resulted from the rise of cyanobacteria on Earth. This estimate concurs with recent evidence for the appearance of oxygenic photosynthetic organisms on Earth, suggesting that low and/or localized levels of photosynthetically produced oxygen necessitated the emergence of ROS scavenging mechanisms to protect life. Life forms have therefore evolved in the presence of ROS on Earth for at least 3.8–3.6 billion years, highlighting the intimate relationship that exists today between many physiological and developmental processes and ROS.

Summary: Systemic 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.