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1. Vascular and nonvascular transmission of systemic reactive oxygen signals during wounding and heat stress

   https://doi.org/10.1093/plphys/kiab157  

   Zandalinas, Sara I ; Mittler, Ron ( April 2021 , Plant Physiology)

   null (Ed.)

   Abstract Sensing of heat, high light (HL), or mechanical injury by a single leaf of a plant results in the activation of different systemic signals that reach systemic tissues within minutes and trigger systemic acquired acclimation (SAA) or systemic wound responses (SWRs), resulting in a heightened state of stress readiness of the entire plant. Among the different signals associated with rapid systemic responses to stress in plants are electric, calcium, and reactive oxygen species (ROS) waves. These signals propagate from the stressed or injured leaf to the rest of the plant through the plant vascular bundles, and trigger SWRs and SAA in systemic tissues. However, whether they can propagate through other cell types, and whether or not they are interlinked, remain open questions. Here we report that in response to wounding or heat stress (HS), but not HL stress, the ROS wave can propagate through mesophyll cells of Arabidopsis (Arabidopsis thaliana). Moreover, we show that ROS production by mesophyll cells during these stresses is sufficient to restore SWR and SAA transcript accumulation in systemic leaves, as well as SAA to HS (but not HL). We further show that propagation of the ROS wave through mesophyll cells could contribute to systemic signal integration during HL and HS stress combination. Our findings reveal that the ROS wave can propagate through tissues other than the vascular bundles of plants, and that different stresses can trigger different types of systemic signals that propagate through different cell layers and induce stress-specific systemic responses. 

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2. Jasmonic acid and salicylic acid modulate systemic reactive oxygen species signaling during stress responses

   https://doi.org/10.1093/plphys/kiac449  

   Myers, Jr, Ronald J. ; Fichman, Yosef ; Zandalinas, Sara I. ; Mittler, Ron ( September 2022 , Plant Physiology)

   Plants can send long-distance cell-to-cell signals from a single tissue subjected to stress to the entire plant. This ability is termed “systemic signaling” and is essential for plant acclimation to stress and/or defense against pathogens. Several signaling mechanisms are associated with systemic signaling, including the reactive oxygen species (ROS) wave, calcium wave, hydraulic wave, and electric signals. The ROS wave coordinates multiple physiological, molecular, and metabolic responses among different parts of the plant and is essential for systemic acquired acclimation (SAA) to stress. In addition, it is linked with several plant hormones, including jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA). However, how these plant hormones modulate the ROS wave and whether they are required for SAA is not clear. Here we report that SA and JA play antagonistic roles in modulating the ROS wave in Arabidopsis (Arabidopsis thaliana). While SA augments the ROS wave, JA suppresses it during responses to local wounding or high light (HL) stress treatments. We further show that ethylene and ABA are essential for regulation of the ROS wave during systemic responses to local wounding treatment. Interestingly, we found that the redox-response protein NONEXPRESSOR OF PATHOGENESIS RELATED PROTEIN 1 is required for systemic ROS accumulation in response to wounding or HL stress, as well as for SAA to HL stress. Taken together, our findings suggest that interplay between JA and SA might regulate systemic signaling and SAA during responses of plants to abiotic stress or wounding.

    

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3. Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants

   https://doi.org/10.1111/tpj.15360  

   Fichman, Yosef ; Mittler, Ron ( June 2021 , The Plant Journal)

   The sensing of abiotic stress, mechanical injury or pathogen attack by a single plant tissue results in the activation of systemic signals that travel from the affected tissue to the entire plant. This process is essential for plant survival during stress and is termed systemic signaling. Among the different signals triggered during this process are calcium, electric, reactive oxygen species and hydraulic signals. These are thought to propagate at rapid rates through the plant vascular bundles and to regulate many of the systemic processes essential for plant survival. Although the different signals activated during systemic signaling are thought to be interlinked, their coordination and hierarchy still need to be determined. Here, using a combination of advanced whole‐plant imaging and hydraulic pressure measurements, we studied the activation of all four systemic signals in wild‐type and differentArabidopsis thalianamutants subjected to a local treatment of high‐light (HL) stress or wounding. Our findings reveal that activation of systemic membrane potential, calcium, reactive oxygen species and hydraulic pressure signals, in response to wounding, is dependent on glutamate receptor‐like proteins 3.3 and 3.6. In contrast, in response to HL stress, systemic changes in calcium and membrane potential depended on glutamate receptor‐like 3.3 and 3.6, while systemic hydraulic signals did not. We further show that plasmodesmata functions are required for systemic changes in membrane potential and calcium during responses to HL stress or wounding. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress.

    

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4. Cyclic nucleotide‐gated ion channel 6 is involved in extracellular ATP signaling and plant immunity

   https://doi.org/10.1111/tpj.15636  

   Duong, Ha N. ; Cho, Sung‐Hwan ; Wang, Limin ; Pham, An Q. ; Davies, Julia M. ; Stacey, Gary ( December 2021 , The Plant Journal)

   Extracellular ATP (eATP) is known to act as a danger signal in both plants and animals. In plants, eATP is recognized by the plasma membrane (PM)‐localized receptor P2K1 (LecRK‐I.9). Among the first measurable responses to eATP addition is a rapid rise in cytoplasmic free calcium levels ([Ca²⁺]_cyt), which requires P2K1. However, the specific transporter/channel proteins that mediate this rise in [Ca²⁺]_cytare unknown. Through a forward genetic screen, we identified an Arabidopsis ethylmethanesulfonate (EMS) mutant impaired in the [Ca²⁺]_cytresponse to eATP. Positional cloning revealed that the mutation resided in thecngc6gene, which encodes cyclic nucleotide‐gated ion channel 6 (CNGC6). Mutation of theCNGC6gene led to a notable decrease in the PM inward Ca²⁺current in response to eATP. eATP‐induced mitogen‐activated protein kinase activation and gene expression were also significantly lower incngc6mutant plants. In addition,cngc6mutant plants were also more susceptible to the bacterial pathogenPseudomonas syringae. Taken together, our results indicate that CNGC6 plays a crucial role in mediating eATP‐induced [Ca²⁺]_cytsignaling, as well as plant immunity.

    

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5. Aboveground plant-to-plant electrical signaling mediates network acquired acclimation

   https://doi.org/10.1093/plcell/koac150  

   Szechyńska-Hebda, Magdalena ; Lewandowska, Maria ; Witoń, Damian ; Fichman, Yosef ; Mittler, Ron ; Karpiński, Stanisław M ( May 2022 , The Plant Cell)

   Abstract Systemic acquired acclimation and wound signaling require the transmission of electrical, calcium, and reactive oxygen species (ROS) signals between local and systemic tissues of the same plant. However, whether such signals can be transmitted between two different plants is largely unknown. Here, we reveal a new type of plant-to-plant aboveground direct communication involving electrical signaling detected at the surface of leaves, ROS, and photosystem networks. A foliar electrical signal induced by wounding or high light stress applied to a single dandelion leaf can be transmitted to a neighboring plant that is in direct contact with the stimulated plant, resulting in systemic photosynthetic, oxidative, molecular, and physiological changes in both plants. Furthermore, similar aboveground changes can be induced in a network of plants serially connected via touch. Such signals can also induce responses even if the neighboring plant is from a different plant species. Our study demonstrates that electrical signals can function as a communication link between transmitter and receiver plants that are organized as a network (community) of plants. This process can be described as network-acquired acclimation. 

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