More Like this

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. 

   more » « less
2. Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis

   https://doi.org/10.1126/scisignal.abf0322  

   Fichman, Yosef ; Myers, Ronald J. ; Grant, DeAna G. ; Mittler, Ron ( February 2021 , Science Signaling)

   null (Ed.)

   Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (the local tissue) to the entire plant (systemic tissues). Reactive oxygen species (ROS) and Ca 2+ are key signaling molecules thought to be involved in this cell-to-cell mechanism. Here, we report that the systemic response of Arabidopsis thaliana to a local treatment of high light stress, which resulted in local ROS accumulation, required ROS generated by respiratory burst oxidase homolog D (RBOHD). ROS increased cell-to-cell transport and plasmodesmata (PD) pore size in a manner dependent on PD-localized protein 1 (PDLP1) and PDLP5, and this process was required for the propagation of the systemic ROS signals and SAA. Furthermore, aquaporins and several Ca 2+ -permeable channels in the glutamate receptor–like (GLR), mechanosensitive small conductance–like (MSL), and cyclic nucleotide–gated (CNGC) families were involved in this systemic signaling process. However, we determined that these channels were required primarily to amplify the systemic signal in each cell along the path of the systemic ROS wave, as well as to establish local and systemic acclimation. Thus, PD and RBOHD-generated ROS orchestrate light stress–induced rapid cell-to-cell spread of systemic signals in Arabidopsis . 

   more » « less
3. HPCA1 is required for systemic reactive oxygen species and calcium cell-to-cell signaling and plant acclimation to stress

   https://doi.org/10.1093/plcell/koac241  

   Fichman, Yosef ; Zandalinas, Sara I. ; Peck, Scott ; Luan, Sheng ; Mittler, Ron ( August 2022 , The Plant Cell)

   Reactive oxygen species (ROS), produced by respiratory burst oxidase homologs (RBOHs) at the apoplast, play a key role in local and systemic cell-to-cell signaling, required for plant acclimation to stress. Here we reveal that the Arabidopsis thaliana leucine-rich-repeat receptor-like kinase H2O2-INDUCED CA2+ INCREASES 1 (HPCA1) acts as a central ROS receptor required for the propagation of cell-to-cell ROS signals, systemic signaling in response to different biotic and abiotic stresses, stress responses at the local and systemic tissues, and plant acclimation to stress, following a local treatment of high light (HL) stress. We further report that HPCA1 is required for systemic calcium signals, but not systemic membrane depolarization responses, and identify the calcium-permeable channel MECHANOSENSITIVE ION CHANNEL LIKE 3, CALCINEURIN B-LIKE CALCIUM SENSOR 4 (CBL4), CBL4-INTERACTING PROTEIN KINASE 26 and Sucrose-non-fermenting-1-related Protein Kinase 2.6/OPEN STOMATA 1 (OST1) as required for the propagation of cell-to-cell ROS signals. In addition, we identify serine residues S343 and S347 of RBOHD (the putative targets of OST1) as playing a key role in cell-to-cell ROS signaling in response to a local application of HL stress. Our findings reveal that HPCA1 plays a key role in mediating and coordinating systemic cell-to-cell ROS and calcium signals required for plant acclimation to stress.

    

   more » « less
4. Rapid systemic responses of Arabidopsis to waterlogging stress

   https://doi.org/10.1093/plphys/kiad433  

   Peláez-Vico, María Ángeles ; Tukuli, Adama ; Singh, Pallav ; Mendoza-Cózatl, David G ; Joshi, Trupti ; Mittler, Ron ( August 2023 , Plant Physiology)

   Waterlogging stress (WLS) negatively impacts the growth and yield of crops resulting in heavy losses to agricultural production. Previous studies have revealed that WLS induces a systemic response in shoots that is partially dependent on the plant hormones ethylene and abscisic acid. However, the role of rapid cell-to-cell signaling pathways, such as the reactive oxygen species (ROS) and calcium waves, in systemic responses of plants to WLS is unknown at present. Here, we reveal that an abrupt WLS treatment of Arabidopsis (Arabidopsis thaliana) plants growing in peat moss triggers systemic ROS and calcium wave responses and that the WLS-triggered ROS wave response of Arabidopsis is dependent on the ROS-generating RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD), calcium-permeable channels GLUTAMATE-LIKE RECEPTOR 3.3 and 3.6 (GLR3.3 and GLR3.6), and aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN 2;1 (PIP2;1) proteins. We further show that WLS is accompanied by a rapid systemic transcriptomic response that is evident as early as 10 min following waterlogging initiation, includes many hypoxia-response transcripts, and is partially dependent on RBOHD. Interestingly, the abrupt WLS of Arabidopsis resulted in the triggering of a rapid hydraulic wave response and the transient opening of stomata on leaves. In addition, it induced in plants a heightened state of tolerance to a subsequent submergence stress. Taken together, our findings reveal that the initiation of WLS in plants is accompanied by rapid systemic physiological and transcriptomic responses that involve the ROS, calcium, and hydraulic waves, as well as the induction of hypoxia acclimation mechanisms in systemic tissues.

    

   more » « less
5. 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.

    

   more » « less