Coordinating the overall stomatal response of plants: Rapid leaf-to-leaf communication during light stress

Abstract

The plant canopy functions as an aerial array of light-harvesting antennas. To achieve maximal yield, each leaf within this array and the array as a whole need to rapidly adjust to naturally occurring fluctuations in light intensity and quality. Excessive light stress triggers the closing of pores in leaves called stomata to minimize moisture loss. We found that different leaves within the canopy of an plant, including leaves not directly exposed to light, coordinated stomatal closure in response to light stress by sending and receiving rapid systemic signals. This response required the plant hormones abscisic acid and jasmonic acid and was mediated by a rapid autopropagating wave of reactive oxygen species (ROS) production. Furthermore, this response depended on the function of genes encoding the ROS-generating NADPH oxidase RBOHD and various stomatal regulators, such as the anion channel SLAC1, GHR1 (guard cell hydrogen peroxide resistant 1), and lipoxygenase 1 (LOX1). Our findings reveal that plants function as highly dynamic and coordinated organisms, optimizing the overall response of their canopies to fluctuating light intensities.

Coordinated and rapid whole‐plant systemic stomatal responses

“…a–d; Supporting Information Methods S1). While heat stress and dark‐to‐light transition initiated a rapid local and systemic stomatal opening responses, wounding induced rapid local and systemic stomatal closure responses, similar to the light stress‐induced local and systemic responses previously reported (Devireddy et al ., ). Taken together, the results shown in Fig.…”

“…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. i; Devireddy et al ., ). As shown in Fig.…”

“…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. k), potentially suggesting that systemic stomatal responses to light stress could be associated with pathogen‐induced stomatal closure pathways (Chen et al ., ; Devireddy et al ., ; David et al ., ; Kollist et al ., ). The findings presented in Fig.…”

“…Rapid alterations in stomatal aperture were previously shown to regulate leaf temperature, rates of CO 2 exchange, water vapor loss and responses to pathogen infection (Melotto et al ., ; Vahisalu et al ., ; Raven, ; Guzel Deger et al ., ; Chen et al ., ; Devireddy et al ., ; Yoshida & Fernie, ; Zhang et al ., ; Kollist et al ., ). Here, it is shown that rapid alterations in stomatal aperture (opening or closing) induced by different environmental stimuli in a local leaf trigger a ROS‐dependent systemic signal that alters the stomatal aperture in multiple systemic untreated leaves within minutes (Figs ).…”

Systemic signalling, and the synchronization of stomatal response

“…Additionally, it would be useful to investigate whether there was a systemic signal, such as the ROS wave, by investigating systemic leaf or whole plant ROS changes (e.g. Miller et al , ; Devireddy et al , ). For instance, Fichman et al () showed a whole plant increase in ROS when only one leaf was subject to either wounding or high‐light stress.…”