Systemic signaling during abiotic stress combination in plants

Abstract

<jats:p>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.</jats:p>

Vascular Bundles Mediate Systemic Reactive Oxygen Signaling during Light Stress

“…Plants and other multicellular organisms are able to transmit different chemical and physical signals over long distances, sometimes traversing their entire length. These signals coordinate the response of the entire organism to different stresses, pathogens and/or other stimuli, and are thought to play a key role in the acclimation, defense and adaptation of different organisms to their environment (Kollist et al, 2019;Wang et al, 2019;Takahashi et al, 2018;Choi et al, 2017;Fichman and Mittler, 2020). In plants, a plethora of chemical and physical signals are transmitted from a single leaf or root tip subjected to stress (i.e., a local tissue) to the entire plant (i.e., systemic tissues).…”

“…In recent years, a role for two interlinked signal transduction molecules, i.e., Ca 2+ and ROS, was identified in the systemic response of plants to different abiotic stimuli such as excess light stress or wounding. These two signals were further shown to propagate from cell to cell over long distances in plants and termed the ROS and Ca 2+ waves (Miller et al, 2009;Choi et al, 2014;Fichman et al, 2019;Toyota et al, 2018;Zandalinas and Mittler, 2018;Fichman and Mittler, 2020).…”

“…The ROS wave is essential for coordinating systemic metabolic responses that generate different metabolic signatures in different parts of the plant (Choudhury et al, 2018), for coordinating systemic transcriptomic responses that activate transcriptional networks essential for plant acclimation (Zandalinas et al, 2019), and for coordinating systemic physiological responses, such as changes in stomatal aperture (Devireddy et al, 2018(Devireddy et al, , 2020. In addition, the ROS wave is required for successful plant acclimation to light and heat stresses (Suzuki et al, 2013;Devireddy et al, 2018;Zandalinas et al, 2019Zandalinas et al, , 2020. The initiation, propagation and maintenance of the ROS wave in response to abiotic stress is dependent on the plasma membrane-localized RBOHD (AT5G47910) protein (Miller et al, 2009;Zandalinas and Mittler, 2018;Fichman and Mittler, 2020).…”

“…In addition, the ROS wave is required for successful plant acclimation to light and heat stresses (Suzuki et al, 2013;Devireddy et al, 2018;Zandalinas et al, 2019Zandalinas et al, , 2020. The initiation, propagation and maintenance of the ROS wave in response to abiotic stress is dependent on the plasma membrane-localized RBOHD (AT5G47910) protein (Miller et al, 2009;Zandalinas and Mittler, 2018;Fichman and Mittler, 2020). However, genetic evidence in the form of complementation studies, as well as cell biology studies elucidating the role of RBOHD in different plant tissues during systemic signaling, have thus far been lacking.…”

Coordinated Systemic Stomatal Responses in Soybean

“…Systemic stomatal responses in Arabidopsis depend on systemic reactive oxygen species (ROS) signals and include systemic stomatal closure responses to light or wounding, as well as systemic stomatal opening responses to heat (Devireddy et al, 2018(Devireddy et al, , 2020Kollist et al, 2019;Zandalinas et al, 2020a). The systemic stomatal response of soybean appeared to occur at a rate comparable to that of Arabidopsis (6 min to transverse ;25-cm distance; Fig.…”