Glutathionylation and Reduction of Methacrolein in Tomato Plants Account for Its Absorption from the Vapor Phase

• Published in: Plant physiology (Bethesda) 2015-11, Vol.169 (3), p.1744-1754
• Main Authors: Muramoto, Shoko, Matsubara, Yayoi, Mwenda, Cynthia Mugo, Koeduka, Takao, Sakami, Takuya, Tani, Akira, Matsui, Kenji
• Format: Article
• Language: English
• Subjects: Absorption, Physicochemical - physiology; Acrolein - analogs & derivatives; Acrolein - chemistry; Acrolein - metabolism; Adducts; Alcohols; Biodegradation, Environmental; Butadienes - chemistry; Enzymes; FOCUS ON METABOLISM; Glutathione - chemistry; Glutathione - metabolism; Hemiterpenes - chemistry; Ketones; Leaves; Lycopersicon esculentum - chemistry; Lycopersicon esculentum - metabolism; Metabolism; Oxidation-Reduction; Oxygen - chemistry; Pentanes - chemistry; Photosynthesis; Plant Leaves - chemistry; Plant tissues; Plants; s - Focus Issue; Vapors; Volatile organic compounds; Volatile Organic Compounds - chemistry; Volatile Organic Compounds - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.15.01045

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.