Ozone inhibits guard cell K ⁺ channels implicated in stomatal opening

Abstract

Ozone (O3) deleteriously affects organisms ranging from humans to crop plants, yet little is understood regarding the underlying mechanisms. In plants, O3 decreases CO2 assimilation, but whether this could result from direct O 3 action on guard cells remained unknown. Potassium flux causes osmotically driven changes in guard cell volume that regulate apertures of associated microscopic pores through which CO 2 is supplied to the photosynthetic mesophyll tissue. We show in Vicia faba that O3 inhibits (i) guard cell K ؉ channels that mediate K ؉ uptake that drives stomatal opening; (ii) stomatal opening in isolated epidermes; and (iii) stomatal opening in leaves, such that CO2 assimilation is reduced without direct effects of O 3 on photosynthetic capacity. Direct O3 effects on guard cells may have ecological and agronomic implications for plant productivity and for response to other environmental stressors including drought.

The Role of Reactive Oxygen Species in Hormonal Responses

“…Similarly, ozone causes secondary ROS production in guard cells and inhibits outward and inward K 1 channels (Torsethaugen et al, 1999;Joo et al, 2005). Ozone inhibits stomatal opening, but does not inhibit stomatal closing (Torsethaugen et al, 1999). The residual outward K 1 currents after ROS application may be sufficient to function in K 1 efflux during stomatal closing, as previous analyses have shown that roughly 25% of K 1 channel activities are sufficient for physiological K 1 fluxes during stomatal movements (Schroeder et al, 1984;Kelly et al, 1995;Kwak et al, 2001).…”

“…Interestingly, outward K 1 channels are inhibited by H 2 O 2 , which could cause inhibition of ABA and/or ROS-induced stomatal closure (Torsethaugen et al, 1999;Zhang et al, 2001b;Kö hler et al, 2003). Similarly, ozone causes secondary ROS production in guard cells and inhibits outward and inward K 1 channels (Torsethaugen et al, 1999;Joo et al, 2005).…”

“…Similarly, ozone causes secondary ROS production in guard cells and inhibits outward and inward K 1 channels (Torsethaugen et al, 1999;Joo et al, 2005). Ozone inhibits stomatal opening, but does not inhibit stomatal closing (Torsethaugen et al, 1999).…”

Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling in Plants

“…ABA-stimulated ROS accumulation induces stomatal closure via activation of plasma membrane calcium channels (Pei et al, 2000), and changes in intracellular calcium levels were shown to mediate stomatal closure triggered by application of H 2 O 2 or the herbicide methyl viologen, which generates superoxide in chloroplasts (McAinsh et al, 1996). Complementary to the calcium-mediated stomatal closure triggered by H 2 O 2 , ozone exerts its function by inhibiting guard cell potassium channels that assist potassium uptake, which in turn drives stomatal opening (Torsethaugen et al, 1999). There is evidence for MAPKs to be involved in stomata regulation; NtMPK4 is preferentially expressed in the epidermis and NtMPK4-silenced plants are hypersensitive to ozone due to an ABA-independent misregulation of stomatal closure (Gomi et al, 2005).…”

Studying guard cells in the intact plant: modulation of stomatal movement by apoplastic factors

“…They are susceptible to stimuli from both sides and are capable of processing information from various sources. Guard cells are sensitive to light, CO 2 , temperature, the phytohormones abscisic acid (ABA) and auxin (Assmann, 1993) as well as reactive oxygen species (Torsethaugen et al , 1999;Pei et al , 2000). The mechanism by which guard cells integrate these signals to trigger stomatal movement is not understood in detail, yet.…”