Glutathionylation and reduction of methacrolein in tomato plants account for its absorption from the vapor phase

Abstract

A large portion of the volatile organic compounds emitted by plants are oxygenated to yield reactive carbonyl species, which have a big impact on atmospheric chemistry. Deposition to vegetation driven by the absorption of reactive carbonyl species into plants plays a major role in cleansing the atmosphere, but the mechanisms supporting this absorption have been little examined.Here, we performed model experiments using methacrolein (MACR), one of the major reactive carbonyl species formed from isoprene, and tomato (Solanum lycopersicum) plants. Tomato shoots enclosed in a jar with MACR vapor efficiently absorbed MACR. The absorption efficiency was much higher than expected from the gas/liquid partition coefficient of MACR, indicating that MACR was likely metabolized in leaf tissues. Isobutyraldehyde, isobutyl alcohol, and methallyl alcohol (MAA) were detected in the headspace and inside tomato tissues treated with MACR vapor, suggesting that MACR was enzymatically reduced. Glutathione (GSH) conjugates of MACR (MACR-GSH) and MAA (MAA-GSH) were also detected. MACR-GSH was essentially formed through spontaneous conjugation between endogenous GSH and exogenous MACR, and reduction of MACR-GSH to MAA-GSH was likely catalyzed by an NADPH-dependent enzyme in tomato leaves. Glutathionylation was the metabolic pathway most responsible for the absorption of MACR, but when the amount of MACR exceeded the available GSH, MACR that accumulated reduced photosynthetic capacity. In an experiment simulating the natural environment using gas flow, MACR-GSH and MAA-GSH accumulation accounted for 30% to 40% of the MACR supplied. These results suggest that MACR metabolism, especially spontaneous glutathionylation, is an essential factor supporting MACR absorption from the atmosphere by tomato plants.

A mechanism for biogenic production and emission of MEK from MVK decoupled from isoprene biosynthesis

“…MACR was also efficiently metabolized, consistent with other literature reports on tomato plants (Muramoto et al, 2015). In this case, however, detected volatiles produced by MACR reduction represented only about 9 % of the MACR uptake.…”

“…However, only a transient release of such products was detected. Isobutyraldehyde emission accounted for 6.5 % of the MACR uptake within 2 h, confirming results from a previous study on tomato plants (6.4 %; Muramoto et al, 2015). Muramoto et al (2015) reported that most MACR in the leaf undergoes glutathionylation.…”

“…The observation that no 13 C labelling appeared in any of the emitted carbonyls suggests that isoprene is not involved in their biosynthesis. We are not aware of isoprene pools that label slowly in plants (Niinemets et al, 2004). However, sources independent of freshly assimilated carbon contribute to isoprene production when photosynthesis is stress-constrained (Brilli et al, 2007).…”

“…Plants also rapidly take up MACR and MVK (Andreae et al, 2002;Karl et al, 2004Karl et al, , 2005Karl et al, , 2010, suggesting that these compounds may be metabolized. Detoxification mechanisms for MACR have been reported (Muramoto et al, 2015), whereas this is not the case for MVK.…”

Technical note: Conversion of isoprene hydroxy hydroperoxides (ISOPOOHs) on metal environmental simulation chamber walls

“…The vapor pressure of ISOPOOH is about 3 orders of magnitude lower than that of MVK and MACR, and that of IEPOX is even lower, which increases the importance of their partitioning to surfaces and the condensed phase (Rivera-Rios et al, 2014). ISOPOOH and IEPOX have been shown to play an important role in SOA formation and reactive uptake (Bates et al, 2014;Gaston et al, 2014;Krechmer et al, 2015;Nguyen et al, 2014a).…”