Guard Cells Integrate Light and Temperature Signals to Control Stomatal Aperture

Abstract

High temperature promotes guard cell expansion, which opens stomatal pores to facilitate leaf cooling. How the hightemperature signal is perceived and transmitted to regulate stomatal aperture is, however, unknown. Here, we used a reverse-genetics approach to understand high temperature-mediated stomatal opening in Arabidopsis (Arabidopsis thaliana). Our findings reveal that high temperature-induced guard cell movement requires components involved in blue lightmediated stomatal opening, suggesting cross talk between light and temperature signaling pathways. The molecular players involved include phototropin photoreceptors, plasma membrane H 1-ATPases, and multiple members of the 14-3-3 protein family. We further show that phototropin-deficient mutants display impaired rosette evapotranspiration and leaf cooling at high temperatures. Blocking the interaction of 14-3-3 proteins with their client proteins severely impairs high temperatureinduced stomatal opening but has no effect on the induction of heat-sensitive guard cell transcripts, supporting the existence of an additional intracellular high-temperature response pathway in plants.

Keep Cool and Open Up: Temperature-Induced Stomatal Opening

“…However, the stomatal response to high temperatures occurs in darkness as well, confirming the contributions of additional thermosensing mechanisms in the guard cells. Kostaki et al (2020) do not confirm which steps of blue light-mediated stomatal opening are temperature sensitive, but their data support the existence of a sensing mechanism alongside the phyB cascade. The detailed mechanisms, particularly how they are involved in stomatal opening, remain speculative (Fig.…”

“…These traits all help a plant to adapt to a warm environment as the plant develops. By contrast, the stomatal opening phenotype described by Kostaki et al (2020) is rapid and plastic, and probably the earliest response to elevated temperature. This rapid response might therefore require a reversible sensing mechanism that can be switched off when temperatures decrease again.…”

“…However, this does not match the loss of warmth-induced stomatal opening in phot1 phot2 loss-of-function plants. As noted by Kostaki et al (2020), the thermosensitive function of the phototropins requires activation by blue light. However, the stomatal response to high temperatures occurs in darkness as well, confirming the contributions of additional thermosensing mechanisms in the guard cells.…”

“…Stomata can additionally help leaf cooling by transpiration. In this issue of Plant Physiology, Kostaki et al (2020) establish that stomatal aperture is quickly enhanced upon exposure to high temperatures, resulting in a significant reduction in leaf temperature. They demonstrate that this is an epidermis-autonomous response that does not act via the known temperature signaling pathways.…”

“…Does the location of the sensor system matter? The stomatal phenotype described by Kostaki et al (2020) is clearly localized and guard cell-autonomous, occurring even in isolated epidermal tissue. Does that mean that it does not receive any input from the underlying tissues?…”