Search for: All records

Abstract Extracellular ATP (eATP) and L-Glutamic acid (L-Glu) are important damage-associated molecular pattern (DAMP) molecules released from cells during injury. Both molecules trigger wound-associated signal transduction pathways, as well as the enhanced production of reactive oxygen species (ROS) by the RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) protein. However, whether eATP and L-Glu trigger overlapping or distinct pathways is mostly unknown. Here, we report that Arabidopsis (Arabidopsis thaliana) responses to eATP or L-Glu are distinct from each other in terms of tissue specificity and transcriptomic responses. Thus, although both DAMPs trigger the expression of multiple wounding and hormone response transcripts in systemic tissues, eATP and L-Glu-induced transcripts have little overlap between them. We further show that wounding of different tissues may result in ROS responses that are controlled by different DAMP receptors. Thus, activation of ROS production following injury of non-vascular tissues primarily depended on the eATP receptors PURINORECEPTOR 2 KINASE 1 and 2 (P2K1P2K2), while activation of ROS responses in vascular tissues following injury primarily depended on the L-Glu receptors GLU-LIKE RECEPTORS 3.3 and 3.6 (GLR3.3GLR3.6). Interestingly, we found that in the absence of the GLR3.3GLR3.6 receptors (ie, in the glr3.3glr3.6 double mutant), the ROS response to eATP application is enhanced. This finding suggests that the L-Glu pathway may suppress the eATP pathway during wounding. Taken together, our findings suggest that the DAMP molecules eATP and L-Glu have complex interactions that appear to be both partly complementary and partly antagonistic, as well as tissue dependent. 

Nitric oxide (NO) is a key regulator of plant development, growth, and responses to the environment. Together with hydrogen peroxide (H₂O₂), NO modifies the structure and function of proteins, controlling redox signaling. Although NO has been studied extensively at the cellular and subcellular levels, very little is known about changes in NO content at the whole‐plant level.Here, we report on the development of an aboveground whole‐plant live imaging method for NO. Using mutants with altered NO levels, as well as an NO donor/scavenger, we demonstrate the specificity of the detection method for NO.Arabidopsis thalianaplants were found to produce a basal level of NO under control conditions. NO levels accumulated enzymatically in plants following heat stress applied to the entire plant, as well as in a systemic manner following different locally applied stimuli. Similar or opposing accumulation patterns were also found for NO and H₂O₂during the response of plants to different stimuli.Our findings reveal that NO accumulates during the systemic response of plants to a local stimulus. In addition, they shed new light on the intricate relationships between NO and H₂O₂. The new method reported opens the way for multiple future studies of NO's role in plant biology. 

Research and innovation in metabolomics tools to measure metabolite accumulation within plants have led to important discoveries with respect to the improvement of plant stress tolerance, development, and crop yield. Traditional metabolomics analyses have commonly utilized gas chromatography–mass spectrometry and liquid chromatography–mass spectrometry, but these methods are often performed without regard for the spatial locations of metabolites within tissues. Methods for mass spectral imaging (MSI) have recently been developed to detect and spatially resolve metabolite accumulation and are rapidly being adopted on a wider scale. Since 2010, the number of publications incorporating mass spectral imaging has grown from approximately 80 articles to over 378 on a yearly basis, constituting an increase of at least 350% during this time frame. Spatially resolved metabolite accumulation data provides unique insights into the function and regulation of plant biochemical pathways. Mass spectral imaging is commonly paired with desorption ionization technologies, including matrix-assisted laser desorption ionization (MALDI) and desorption electrospray ionization (DESI), to generate accurate, spatially resolved metabolomics data from prepared tissue segments. Here, we describe the most recent advancements in sample preparation methods, mass spectral imaging technologies, and data processing tools that have been developed to address the limits of MSI technology. Additionally, we summarize recent applications of MSI technologies in plant metabolomics and discuss potential avenues for future research advancements within the plant biology community through the use of these technologies. 

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. 

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 Mechanical wounding occurs in plants during biotic or abiotic stresses and is associated with the activation of long-distance signaling pathways that trigger wound responses in systemic tissues. Among the different systemic signals activated by wounding are electric signals, calcium, hydraulic, and reactive oxygen species (ROS) waves. The release of glutamate (Glu) from cells at the wounded tissues was recently proposed to trigger systemic signal transduction pathways via GLU-LIKE RECEPTORs (GLRs). However, the role of another important compound released from cells during wounding (extracellular ATP [eATP]) in triggering systemic responses is not clear. Here, we show in Arabidopsis (Arabidopsis thaliana) that wounding results in the accumulation of nanomolar levels of eATP and that these levels are sufficient to trigger the systemic ROS wave. We further show that the triggering of the ROS wave by eATP during wounding requires the PURINORECEPTOR 2 KINASE (P2K) receptor. Application of eATP to unwounded leaves triggered the ROS wave, and the activation of the ROS wave by wounding or eATP application was suppressed in mutants deficient in P2Ks (e.g. p2k1-3, p2k2, and p2k1-3p2k2). In addition, expression of systemic wound response (SWR) transcripts was suppressed in mutants deficient in P2Ks during wounding. Interestingly, the effect of Glu and eATP application on ROS wave activation was not additive, suggesting that these two compounds function in the same pathway to trigger the ROS wave. Our findings reveal that in addition to sensing Glu via GLRs, eATP sensed by P2Ks plays a key role in the triggering of SWRs in plants. 

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 .