Plasmodesmata-localized proteins and ROS orchestrate light-induced rapid systemic signaling in Arabidopsis

Abstract

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 Ca2+ 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 Ca2+-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.

Photosynthesis-independent production of reactive oxygen species in the rice bundle sheath during high light is mediated by NADPH oxidase

“…We were not able to confirm that NADPH oxidase activity is strongest in BSS, so it is possible that they produce the ROS in the mesophyll and that aquaporins then transport ROS to the bundle sheath. If true, this would be analogous to the role of aquaporins in mediating the long-distance high-light systemic signal (27). However, it does appear that specific isoforms of NADPH oxidase are responsible for this high-light response.…”

“…Such ROSmediated systemic signaling from a locally perturbed leaf can lead to stomatal aperture being altered in distant leaves, is associated with the hormones abscisic and jasmonic acid, and is dependent on the plasma membrane-localized NADPH oxidase (AtRBOHD and AtRBOHF) in cells of the phloem and xylem (22)(23)(24)(25)(26). Grafting experiments indicate that the initial local propagation of ROS is dependent on respiratory burst oxidase homolog (RBOH) proteins as well as increased cell-to-cell transport that is dependent on plasmodesmata-localized proteins 1 and 5 as well as aquaporins and Ca 2+ -permeable channels in the glutamate receptor-like, mechanosensitive small conductance-like, and cyclic nucleotide-gated families (27).…”

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

“…Among the different signaling processes thought to mediate such rapid long distance cell‐to‐cell signal transduction mechanisms in plants are changes in membrane potentials (i.e., electric waves; Farmer et al ., 2020; Hedrich and Fukushima, 2021; Mousavi et al ., 2013; Nguyen et al ., 2018; Shao et al ., 2020; Szechyńska‐Hebda et al ., 2010), steady‐state levels of calcium (i.e., calcium wave; Choi et al ., 2014; Choi et al ., 2017; Dubiella et al ., 2013; Evans et al ., 2016; Shao et al ., 2020; Tian et al ., 2020; Toyota et al ., 2018), steady‐state levels of reactive oxygen species (ROS; i.e., ROS wave; Fichman et al ., 2019; Fichman and Mittler, 2020b; Kollist et al ., 2019; Lew et al ., 2020; Miller et al ., 2009; Mittler et al ., 2011; Zandalinas et al ., 2019; Zandalinas et al ., 2020a; Zandalinas et al ., 2020b), hydraulic pressure (i.e., hydraulic wave; Christmann et al ., 2013; Malone, 1992; Sade et al ., 2014), as well as rapid changes in the levels of different plant hormones such as jasmonic acid (JA), abscisic acid (ABA) and auxin (Devireddy et al ., 2018; Galvez‐Valdivieso et al ., 2009; Guo et al ., 2016; Kangasjärvi et al ., 2009; Wang et al ., 2019), small peptides (Takahashi et al ., 2018), redox levels (Fichman and Mittler, 2021), and/or different metabolites/metabolic signatures (Choudhury et al ., 2018). Recent studies demonstrated that many of these signals propagate from cell‐to‐cell through the vascular bundles of plants using tissues such as xylem parenchyma and phloem cells to mediate systemic electric, calcium and ROS signals, and xylem cells to mediate hydraulic pressure signals (Christmann et al ., 2013; Fichman et al ., 2021; Mousavi et al ., 2013; Nguyen et al ., 2018; Shao et al ., 2020; Toyota et al ., 2018; Zandalinas et al ., 2020a; Zandalinas et al ., 2020b; Zandalinas and Mittler, 2021). In addition, the calcium channels glutamate receptor‐like (GLR) 3.3 and 3.6 were found to pla...…”

The receptor kinase SRF3 coordinates iron-level and flagellin dependent defense and growth responses in plants

“…However, it is possible that callose deposition might impact later responses since callose deposition-mediated plasmodesmata closure can take hours to days to occur 38,[50][51][52][53] . Another possibility is that callose deposition might have a different function early-on, for instance early ROS signaling which is thought to mediate callose deposition, actually increases cell-to-cell communication in leaves 54 .…”