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Abstract In plants, both developmental processes and environmental responses are spatiotemporally regulated by an assembly of signaling molecules such as hormones, secondary metabolites, and ions. The ability of these signaling molecules to move within and across plant tissues is essential for various developmental cues. However, the characterization of transported signaling molecules and their translocation mechanisms is difficult due to the functional redundancy of plant genomes and shortcomings in methodologies. Here, we report our development of the Multi Targeted AmiRNA Cell type–specific Transportome-scale (mTACT) toolbox, which can be used to reveal phenotypic plasticity in plants. mTACT is based on a large set of artificial microRNAs (amiRNAs), each designed to optimally target multiple members of a particular gene family encoding transporter proteins. In total, the mTACT toolbox includes 5,565 amiRNAs, targeting 81.7% of the Arabidopsis (Arabidopsis thaliana) transportome. The amiRNA library can be driven under 12 cell type–specific promoters, allowing the design of spatial-specific genetic screens. mTACT is further divided into 8 sublibraries of amiRNAs targeting a functionally defined protein class. A proof-of-concept screen validated the mTACT approach by identifying phenotypes linked to both known and unidentified genes. With the ability to overcome functional redundancy in a transportome-scale, cell type–specific manner, the mTACT toolbox will allow the plant research community to study previously hidden genetic factors required for long- and short-distance translocation of signaling molecules. 

Abstract Reactive oxygen species (ROS) play a critical role in plant development and stress responses, acting as key components in rapid signalling pathways. The ‘ROS wave’ triggers essential acclimation processes, ultimately ensuring plant survival under diverse challenges. This review explores recent advances in understanding the composition and functionality of the ROS wave within plant cells. During their initiation and propagation, ROS waves interact with other rapid signalling pathways, hormones and various molecular compounds. Recent research sheds light on the intriguing lack of a rigid hierarchy governing these interactions, highlighting a complex interplay between diverse signals. Notably, ROS waves culminate in systemic acclimation, a crucial outcome for enhanced stress tolerance. This review emphasizes the versatility of ROS, which act as flexible players within a network of short‐ and long‐term factors contributing to plant stress resilience. Unveiling the intricacies of these interactions between ROS and various signalling molecules holds immense potential for developing strategies to augment plant stress tolerance, contributing to improved agricultural practices and overall ecosystem well‐being. 

Two plants connected via a Cuscuta bridge exchange rapid systemic calcium, electric, and reactive oxygen species signals, suggesting that Cuscuta may have beneficial effects to host plants. 

Cell-to-cell communication is fundamental to multicellular organisms and unicellular organisms living in a microbiome. It is thought to have evolved as a stress- or quorum-sensing mechanism in unicellular organisms. A unique cell-to-cell communication mechanism that uses reactive oxygen species (ROS) as a signal (termed the “ROS wave”) was identified in flowering plants. This process is essential for systemic signaling and plant acclimation to stress and can spread from a small group of cells to the entire plant within minutes. Whether a similar signaling process is found in other organisms is however unknown. Here, we report that the ROS wave can be found in unicellular algae, amoeba, ferns, mosses, mammalian cells, and isolated hearts. We further show that this process can be triggered in unicellular and multicellular organisms by a local stress or H₂O₂treatment and blocked by the application of catalase or NADPH oxidase inhibitors and that in unicellular algae it communicates important stress–response signals between cells. Taken together, our findings suggest that an active process of cell-to-cell ROS signaling, like the ROS wave, evolved before unicellular and multicellular organisms diverged. This mechanism could have communicated an environmental stress signal between cells and coordinated the acclimation response of many different cells living in a community. The finding of a signaling process, like the ROS wave, in mammalian cells further contributes to our understanding of different diseases and could impact the development of drugs that target for example cancer or heart disease. 

Abstract 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. 

Abstract 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.