The plant tissues conducting the propagation of rapid systemic responses to wounding and other environmental stimuli have recently been the subject of intense investigation, with increasing evidence pointing to the plant vascular system, and in particular the phloem network, as a key mediator (Kangasjarvi et al., 2009; Choudhury et al., 2018; Nguyen et al., 2018; Toyota et al., 2018 Kollist et al., 2019). To determine whether systemic stomatal responses are mediated via a signal that propagates through the plant vascular system, we measured the kinetics of the stomatal closure response to excess light stress in local and different systemic leaves (Fig. 1e). Interestingly, although the local (treated) leaf is primarily connected to only two to three systemic leaves via the vascular phloem system (Toyota et al., 2018), the rapid systemic stomatal response occurred at an almost similar rate in all systemic leaves measured (with the exception of faster kinetics observed in younger leaves; S4–6), suggesting that the systemic signal mediating rapid systemic stomatal responses to excess light stress is not limited in its transport to vascular phloem cells. Nevertheless, as shown in Fig. 1(f–h), in contrast to the rate of stomatal closure in local leaves, which was similar between stomata located at different parts of the leaf (i.e. stomata in areas A–C; Fig. 1g), the rate of stomatal closure in the different systemic leaves was faster in stomata closest to the midvein (stomata in areas A) and slower in stomata at the periphery of the leaf (stomata in areas B and C; Fig. 1h). The findings presented in Fig. 1(e,f–h) point to a possibility that two different signals are involved in mediating systemic stomatal responses, one that travels through, or is associated with, the vascular system (e.g. ABA; Schachtman & Goodger, 2008; Kangasjarvi et al., 2009; Gorecka et al., 2014; Yoshida & Fernie, 2018), and another that travels rapidly through the entire plant (e.g. the ROS wave; Miller et al., 2009; Mittler et al., 2011). At least when it comes to wounding, it was recently shown that although systemic wound responses were primarily mediated through the phloem and involve glutamic acid signaling, locally applied glutamic acid triggered a whole‐plant glutamate receptor‐like‐dependent systemic calcium wave (Toyota et al., 2018). Excess light and wounding may therefore trigger several different rapid systemic signals (e.g. calcium, ROS electric and/or hydraulic waves) that interact and control different aspects of the plant systemic responses, such as transcript expression, metabolite accumulation and stomatal responses (Gorecka et al., 2014; Devireddy et al., 2018; Yoshida & Fernie, 2018; Kollist et al., 2019; Zandalinas et al., 2019; Fig. 1a–h). It is possible, for example, that the rapid signal that travels throughout the entire plant (ROS/hydraulic/electric/calcium wave) triggers ABA production in the vascular system of systemic leaves and that this ABA (produced by the vascular system of systemic leaves) reaches the stomata of systemic leaves and signals their closure.

Three of the major players thought to be involved in the root‐to‐shoot, or leaf‐to‐leaf, systemic response of plants to different environmental stimuli are ABA, jasmonic acid (JA) and salicylic acid (SA) (Schachtman & Goodger, 2008; Kangasjarvi et al., 2009; Gorecka et al., 2014; Devireddy et al., 2018; Yoshida & Fernie, 2018; David et al., 2019; Förster et al., 2019; Kollist et al., 2019). Although the systemic leaf‐to‐leaf stomatal response to excess light was previously shown to depend on local light‐induced ABA accumulation, which leads to ROS production and the initiation of the ROS wave, the role of open stomata 1 (OST1) in this response was not determined (Devireddy et al., 2018). Here it is shown that rapid local and systemic stomatal responses of Arabidopsis to excess light are dependent on the function of the serine/threonine protein kinase OST1, demonstrating that this systemic response could be dependent on ABA‐derived ROS production via OST1‐respiratory burst oxidase protein D (OST1‐RBOHD)‐mediated signaling, or ABA‐derived OST1–SLAC1 interactions (Fig. 1i; Devireddy et al., 2018). As shown in Fig. 1(j), the rapid excess light‐induced local and systemic stomatal closure responses of Arabidopsis were further suppressed in coronatine insensitive 1 (coi1) and allene oxide synthase (aos) mutants, demonstrating that JA is involved in this response. In contrast to ABA and JA, which were required for stomatal closure in local and systemic leaves, suppression of SA biosynthesis in the SA induction deficient 2 (sid2) mutant only affected stomatal responses in systemic leaves (Fig. 1k), potentially suggesting that systemic stomatal responses to light stress could be associated with pathogen‐induced stomatal closure pathways (Chen et al., 2017; Devireddy et al., 2018; David et al., 2019; Kollist et al., 2019). The findings presented in Fig. 1(i–k), suggest that JA and ABA could interact during local and systemic stomatal responses to excess light. Because rapid systemic responses to excess light or wounding depend on ROS and calcium signaling (Devireddy et al., 2018; Toyota et al., 2018; Kollist et al., 2019), it is possible that JA‐ and ABA‐regulated calcium and ROS concentrations mediate systemic stomatal responses via OST1‐SLAC1 (Murata et al., 2001), and/or calcineurin B‐like protein (CBL)‐CBL‐interacting protein kinase (CIPK)‐GORK modulation (Förster et al., 2019).