On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature

Abstract

Among the volatile organic compounds (VOCs) emitted by plants, some are characteristic of stress conditions, but their biosynthesis and the metabolic and environmental control over the emission are still unclear. We performed experiments to clarify whether (1) the emission following wounding can occur at distance from the wounding site, from VOC pools subjected to metabolic signals; and (2) the emission of biogenic VOCs generated by membrane damage (e.g. consequent to wounding or ozone exposure) can also be induced by exposure to high light and high temperature, recurrent in nature. In Phragmites australis, leaf cutting caused large and rapid bursts of acetaldehyde both at the cutting site and on parts of the cut leaf distant from the cutting site. This emission was preceded by a transient stomatal opening and did not occur in conditions preventing stomatal opening. This suggests the presence of a large pool of leaf acetaldehyde whose release is under stomatal control. VOCs other than isoprene, particularly acetaldehyde and (E)‐2‐hexenal, one of the C‐6 compounds formed by the denaturation of membrane lipids, were released by leaves exposed to high temperature and high light. The high‐temperature treatment (45 °C) also caused a rapid stimulation and then a decay of isoprene emission in Phragmites leaves. Isoprene recovered to the original emission level after suspending the high‐temperature treatment, suggesting a temporary deficit of photosynthetically formed substrate under high temperature. Emission of C‐6 compounds was slowly induced by high temperature, and remained high, indicating that membrane denaturation occurs also after suspending the high‐temperature treatment. Conversely, the emission of C‐6 compounds was limited to the high‐light episode in Phragmites. This suggests that a membrane denaturation may also occur in conditions that do not damage other important plant processes such as the photochemistry of photosynthesis of photoinhibition‐insensitive plants. In the photoinhibition‐sensitive Arabidopsis thaliana mutant NPQ1, a large but transient emission of (E)‐2‐hexenal was also observed a few minutes after the high‐light treatment, indicating extensive damage to the membranes. However, (E)‐2‐hexenal emission was not observed in Arabidopsis plants fumigated with isoprene during the high‐light treatment. This confirms that isoprene can effectively protect cellular membranes from denaturation. Our study indicates that large, though often transient, VOC emissions by plants occur in nature. In particular, we demonstrate that VOCs can be released by much larger tissues than those wounded and that even fluctuations of light and temperature regularly observed in nature can induce their emissions. This knowledge adds information that is useful for the parameterization of the emissions and for the estimate of biogenic VOC load in the atmosphere.