Sara I. Zandalinas,  Yosef Fichman,  Amith R. Devireddy,  Soham Sengupta, Rajeev K. Azad, and Ron Mittler

PNAS June 16, 2020 117 (24) 13810-13820

Significance

Environmental stresses such as heat, drought, and salinity, especially in combination with intense light conditions, can have devastating economical and sociological impacts. Although our knowledge of how each of these stresses affects plants when applied individually is vast, we know very little about how plants acclimate to a combination of different stresses. Here we reveal that plants can integrate different local and systemic signals generated during conditions of stress combination. We further show that the specific part at which plants sense the two co-occurring stresses makes a significant difference in how fast and efficient they acclimate. Our results shed light on how plants acclimate to and survive a combination of different stresses.

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.

See https://www.pnas.org/content/117/24/13810

Figure 2: Plants can integrate two different systemic signals generated simultaneously at two different leaves of the same plant during stress combination. (A) Overlap between the systemic transcriptomic response of plants to a local application of HL, HS, or a combination of heat and light stress simultaneously applied to two different leaves (HL&HS). Venn diagrams for the overlap between the different responses are shown at the bottom for local leaves and at the top for systemic leaves. Black arrows in HL&HS plants represent the number of HL-specific (solid), or HS-specific (dashed) transcripts common between local and systemic leaves. (B) Venn diagrams showing the overlap between stress combination-specific transcripts from local (HL or HS) and systemic leaves. (C) Bar graph showing the percent overlap between the systemic HL&HS response and local HL, HS, HL(HL&HS), or HS(HL&HS) responses. All experiments were repeated at least three times with 40 plants per biological repeat. All transcripts included in the figure were significantly different from controls at P < 0.05 (negative binomial Wald test followed by Benjamini–Hochberg correction). HL(HL&HS) and HS(HL&HS) denote a local HL- or HS- treated leaf of a plant subjected to HS or HL on another local leaf, respectively.