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

Abstract

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 different Arabidopsis thaliana mutants 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.

Relationships Among Arsenic-Related Traits, Including Rice Grain Arsenic Concentration and Straighthead Resistance, as Revealed by Genome-Wide Association

“…It appears, then, that increasing S and GSH within a plant could reduce StHD severity in two ways, by increasing Aschelation and by increasing ROS scavenging. Other elements with known roles in induction of ROS scavenging include Si (Kim et al, 2017), Ca (Fichman and Mittler, 2021), and Cu (Ma et al, 2015).…”

HPCA1 is required for systemic ROS and calcium cell-to-cell signaling and plant acclimation to stress

“…Upon sensing of H 2 O 2 , HPCA1 was found to trigger the accumulation of calcium in the cytosol (Wu et al, 2020). This process could activate another type of cell-to-cell signaling pathway termed the ‘calcium wave’ (dependent on the function of the calcium channels glutamate-like receptor 3.3 and 3.6; GLRs; Evans et al, 2016; Toyota et al, 2018; Shao et al, 2020; Fichman and Mittler, 2021a). To determine whether HPCA1 is also required for systemic cell-to-cell calcium signals, we subjected a single leaf of WT, hpca1-1, and hpca1-2 plants to the same HL stress treatment described above and used Fluo-4-AM as a probe in our live imaging platform (Fichman and Mittler, 2021a) to measure changes in cytosolic calcium levels in local and systemic leaves over a period of 30 min.…”

“…Systemic cell-to-cell calcium and ROS signals were previously proposed to be linked with another type of cell-to-cell signaling, termed the ‘electric wave’ (a rapid depolarization of the plasma membrane, also dependent on the function of GLRs; Mousavi et al, 2013; Nguyen et al, 2018; Farmer et al, 2020; Fichman and Mittler, 2021a). To determine whether HPCA1 is also required for systemic cell-to-cell membrane depolarization signals, we subjected a single leaf of WT, hpca1-1, and hpca1-2 plants to the same HL stress treatment described above and used DiBAC 4 (3) as a probe in our live imaging platform (Fichman and Mittler, 2021a) to measure these changes in local and systemic leaves over a period of 30 min. Interestingly, while the systemic cell-to-cell calcium and ROS signals were suppressed in the hpca1 mutants (Figs.…”

“…Previous studies identified RBOHD, RBOHF, and GLR3.3GLR3.6 as key players in this cell-to-cell response (Miller et al, 2009; Mousavi et al, 2013; Toyota et al, 2018; Shao et al, 2020; Zandalinas et al, 2020b). While RBOHs were shown to mediate ROS production required for cell-to-cell signaling and plant acclimation (Miller et al, 2009; Fichman et al, 2019), GLRs were shown to mediate membrane depolarization and alterations in calcium levels (that could potentially drive ROS production; Mousavi et al, 2013; Evans et al, 2016; Toyota et al, 2018; Nguyen et al, 2018; Shao et al, 2020; Fichman and Mittler, 2021a). Prior studies have also suggested that the function of RBOHs and GLRs is interlinked ( e.g., Fichman and Mittler, 2020a; Fichman and Mittler, 2021a).…”

Plant Immune Memory in Systemic Tissue Does Not Involve Changes in Rapid Calcium Signaling

“…A transient change of the cytoplasmic calcium concentration ([Ca 2+ ] cyt ) is one of the earliest events in plant cells upon pathogen recognition, and many studies applying different calcium indicators reported on distinct [Ca 2+ ] cyt patterns in response to PAMPs, e.g., bacterial flg22 ( Ranf et al, 2011 ; Maintz et al, 2014 ; Seybold et al, 2014 ; Thor and Peiter, 2014 ; Keinath et al, 2015 ; Aldon et al, 2018 ; Tian et al, 2020 ). Furthermore, calcium and calcium signaling being instrumental during defense signal propagation from a local attacked site to systemic parts of a plant has been observed as a spread of a calcium signals through the plant along the vasculature and beyond ( Romeis and Herde, 2014 ; Kiep et al, 2015 ; Nguyen et al, 2018 ; Toyota et al, 2018 ; Shao et al, 2020 ; Fichman and Mittler, 2021 ). However, it is unknown whether [Ca 2+ ] cyt changes contribute to SAR.…”