No abstract

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 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 wholeplant 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.

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.

Short title: Vascular bundles mediate systemic ROS signaling One sentence summary: The reactive oxygen species wave propagates through vascular bundles during the systemic response of Arabidopsis thaliana plants to excess light stress.