Abstract

Treatment by volatile plant hormone methyl jasmonate (MeJA) leads to release of methanol and volatiles of lipoxygenase pathway (LOX volatiles) in a dose-dependent manner, but how the dose dependence is affected by stomatal openness is poorly known. We studied the rapid (0–60 min after treatment) response of stomatal conductance (Gs), net assimilation rate (A), and LOX and methanol emissions to varying MeJA concentrations (0.2–50 mM) in cucumber (Cucumis sativus) leaves with partly open stomata and in leaves with reduced Gs due to drought and darkness. Exposure to MeJA led to initial opening of stomata due to an osmotic shock, followed by MeJA concentration-dependent reduction in Gs, whereas A initially decreased, followed by recovery for lower MeJA concentrations and time-dependent decline for higher MeJA concentrations. Methanol and LOX emissions were elicited in a MeJA concentration-dependent manner, whereas the peak methanol emissions (15–20 min after MeJA application) preceded LOX emissions (20–60 min after application). Furthermore, peak methanol emissions occurred earlier in treatments with higher MeJA concentration, while the opposite was observed for LOX emissions. This difference reflected the circumstance where the rise of methanol release partly coincided with MeJA-dependent stomatal opening, while stronger stomatal closure at higher MeJA concentrations progressively delayed peak LOX emissions. We further observed that drought-dependent reduction in Gs ameliorated MeJA effects on foliage physiological characteristics, underscoring that MeJA primarily penetrates through the stomata. However, despite reduced Gs, dark pretreatment amplified stress-volatile release upon MeJA treatment, suggesting that increased leaf oxidative status due to sudden illumination can potentiate the MeJA response. Taken together, these results collectively demonstrate that the MeJA dose response of volatile emission is controlled by stomata that alter MeJA uptake and volatile release kinetics and by leaf oxidative status in a complex manner.

Highlights

  • Stomata play a vital role in controlling the gas exchange between the intercellular air space and ambient air

  • We suggest that an analogous effect occurs in methyl jasmonate (MeJA)-treated leaves as the treatment initially leads to an osmotic shock and associated water efflux from the mesophyll and epidermal cells and hydropassive stomatal opening and reduction in A (Figure 1A,B)

  • Our experiments demonstrate that the response to MeJA strongly depends on Gs that controls

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Summary

Introduction

Stomata play a vital role in controlling the gas exchange between the intercellular air space and ambient air. Besides producing reactive oxygen species (ROS) as key messengers in mediating stomatal closure to other types of stresses [19,20,21,22], the mechanism leading to the stomatal closure by MeJA has been linked to a typical series of alterations during stomatal closure, including elevation of cytosolic Ca2+ concentration and the depolarized plasma membrane, leading to the efflux of K+ from the guard cells, resulting in the loss of turgor and closure of stomata [23,24,25,26]. Herbivory-dependent JAs and exogenously applied MeJA propagate through the leaf and can impact mesophyll and epidermal cells, potentially directly impacting photosynthetic machinery and altering stomatal openness via mechanisms independent of guard cells [24,25,26,27,28]. In the case of MeJA, hydropassive stomatal responses are expected in the very early phases, 1–10 min after

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