Breaking Bad News: Dynamic Molecular Mechanisms of Wound Response in Plants

Abstract

Recognition and repair of damaged tissue are an integral part of life. The failure of cells and tissues to appropriately respond to damage can lead to severe dysfunction and disease. Therefore, it is essential that we understand the molecular pathways of wound recognition and response. In this review, we aim to provide a broad overview of the molecular mechanisms underlying the fate of damaged cells and damage recognition in plants. Damaged cells release the so-called damage associated molecular patterns to warn the surrounding tissue. Local signaling through calcium (Ca2+), reactive oxygen species (ROS), and hormones, such as jasmonic acid, activates defense gene expression and local reinforcement of cell walls to seal off the wound and prevent evaporation and pathogen colonization. Depending on the severity of damage, Ca2+, ROS, and electrical signals can also spread throughout the plant to elicit a systemic defense response. Special emphasis is placed on the spatiotemporal dimension in order to obtain a mechanistic understanding of wound signaling in plants.

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

“…Systemic signaling pathways play a key role in the successful acclimation of plants to rapid changes in their environment (Suzuki et al ., 2013; Zandalinas et al ., 2019; Fichman et al ., 2020; Zandalinas et al ., 2020a; Zandalinas et al ., 2020b). At least four different signals are thought to mediate systemic signaling in plants in response to abiotic stress and mechanical injury (membrane potential, calcium, ROS and hydraulic; Figures 1–4; Choi et al ., 2017; Farmer et al ., 2020; Fichman and Mittler, 2020b; Johns et al ., 2021; Kollist et al ., 2019; Mittler et al ., 2011; Vega‐Muñoz et al ., 2020). Here we reveal that in response to wounding, systemic changes in membrane potential, calcium levels, ROS and hydraulic pressure require the function of GLR3.3;GLR3.6, while in response to HL the systemic changes in ROS levels can occur in the absence of GLR3.3;GLR3.6 (Figures 1–3 and 7).…”

“…Changes in light intensity, temperature, humidity, and/or herbivore or pathogen attack, for example, activate within seconds different signal transduction pathways that regulate different molecular, metabolic and physiological responses, critical for plant survival during stress (Kollist et al ., 2019; Suzuki et al ., 2015). The sensing of stress, pathogen attack and/or mechanical injury not only induces defense and acclimation responses at the affected plant tissue(s), but also triggers a rapid systemic signal transduction process that alerts all other parts of the plant to the impending change in the environment and/or a pathogen/herbivore attack (Choi et al ., 2017; Farmer et al ., 2020; Fichman and Mittler, 2020b; Johns et al ., 2021; Mittler et al ., 2011; Vega‐Muñoz et al ., 2020). This process was shown to occur in multiple plant species in response to many different stimuli or stress conditions and is termed systemic signaling.…”

“…Because plants lack a nervous system that connects the sensing (i.e., local) tissue with all other plant tissues that did not yet experience the stress/pathogen/stimuli (i.e., systemic tissues), systemic signals in plants must travel from cell‐to‐cell over long distances, sometimes spanning the entire length of the plant (Choi et al ., 2017; Farmer et al ., 2020; Fichman and Mittler, 2020b; Johns et al ., 2021; Mittler et al ., 2011; Vega‐Muñoz et al ., 2020). 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).…”

“…Although many of the rapid systemic signaling mechanisms described above were individually characterized, and the proteins underlying some of them identified, it is unknown at present how they interact with each other and how they respond to different stimuli (Choi et al ., 2017; Farmer et al ., 2020; Fichman and Mittler, 2020b; Johns et al ., 2021; Vega‐Muñoz et al ., 2020). Moreover, studies identifying and characterizing each of the different systemic signals described above were conducted in different laboratories around the world using plants grown under different growth conditions, subjected to different types and degrees of stress treatments, as well as measured using different methods and equipment.…”

Pars Pro Toto: Every Single Cell Matters

“…Even at this single cell level, different hormones and their respective cross-talks are indispensable for damage perception and elicitation of the key downstream responses ( Vega-Muñoz et al, 2020 ). Jasmonic acid (JA) is probably considered to be the most important wounding-responsive phytohormone, as its accumulation can be detected within seconds following damage ( Glauser et al, 2009 ).…”