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.

Highlights

  • 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

  • It was found that each different abiotic stress sensed by the plant will trigger its own abiotic stress-specific systemic signaling and acclimation responses that include the accumulation of many different stress-specific transcripts and metabolites, Significance

  • To study systemic signal integration during stress combination, we subjected a single leaf of Arabidopsis to a local treatment of high light (HL), heat stress (HS), or a combination of light and heat stresses, and studied local and systemic responses (Fig. 1, Table 1, SI Appendix, Fig. S1, and Datasets S1–S9)

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Summary

Introduction

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. | | | abiotic stress reactive oxygen species stress combination systemic | acquired acclimation systemic signaling Abiotic stress conditions, such as heat, salinity, and decreased water availability, can have a devastating impact on plant growth and productivity, potentially resulting in extensive yield losses to agriculture, as well as the collapse of entire ecosystems (1, 2). Successful acclimation of plants to stress conditions requires an efficient, timely, and coordinated response that spans most, if not all, parts and tissues of the plant (3) To achieve such as a coordinated response, plants evolved multiple systemic signaling pathways that allow them to communicate different stress signals from a particular part of the plant, that initially sensed the stress (i.e., local tissue), to the entire plant (i.e., systemic tissue), within minutes (3–15). Once these systemic signals are perceived in the systemic tissues of plants, they induce an acclimation process, termed “systemic acquired acclimation” (SAA) (16), that enables these tissues to withstand the stress even if they did not sense or experience it yet (5, 6, 15)

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