Abstract

Recently, we demonstrated that leaf wounding results in the synthesis of pectin methylesterase (PME), which causes the plant to release methanol into the air. Methanol emitted by a wounded plant increases the accumulation of methanol-inducible gene mRNA and enhances antibacterial resistance as well as cell-to-cell communication, which facilitates virus spreading in neighboring plants. We concluded that methanol is a signaling molecule involved in within-plant and plant-to-plant communication. Methanol is considered to be a poison in humans because of the alcohol dehydrogenase (ADH)-mediated conversion of methanol into toxic formaldehyde. However, recent data showed that methanol is a natural compound in normal, healthy humans. These data call into question whether human methanol is a metabolic waste product or whether methanol has specific function in humans.Here, to reveal human methanol-responsive genes (MRGs), we used suppression subtractive hybridization cDNA libraries of HeLa cells lacking ADH and exposed to methanol. This design allowed us to exclude genes involved in formaldehyde and formic acid detoxification from our analysis. We identified MRGs and revealed a correlation between increases in methanol content in the plasma and changes in human leukocyte MRG mRNA levels after fresh salad consumption by volunteers. Subsequently, we showed that the methanol generated by the pectin/PME complex in the gastrointestinal tract of mice induces the up- and downregulation of brain MRG mRNA. We used an adapted Y-maze to measure the locomotor behavior of the mice while breathing wounded plant vapors in two-choice assays. We showed that mice prefer the odor of methanol to other plant volatiles and that methanol changed MRG mRNA accumulation in the mouse brain.We hypothesize that the methanol emitted by wounded plants may have a role in plant-animal signaling. The known positive effect of plant food intake on human health suggests a role for physiological methanol in human gene regulation.

Highlights

  • Plants are exposed to a different abiotic and biotic stress conditions [1,2,3]

  • We concluded that hGAPDH, hTax1BP1, human sorting nexin family member 27 (hSNX27) and human cyclin A2 (hCycA2) are genes that are sensitive to methanol, which we called methanol-responsive genes (MRGs)

  • Many plants respond to wounding from pathogen and herbivore attacks by releasing airborne volatile compounds that serve as plant defenses involved in within-plant and plant-to-plant signaling, attracting natural enemies of the herbivores and repelling other herbivores [99]

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Summary

Introduction

Plants are exposed to a different abiotic and biotic stress conditions [1,2,3]. Physical damage to a plant is a potential threat because it allows pathogen entry. The mechanical wounding of plant leaves after wind, rain, hail, or herbivore feeding is one of the first steps in pathogen infection and herbivore attack and activates signal transduction pathways and airborne signals to fend off harmful organisms. In response to an attack by a pathogen and plant damage, several plant species emit volatile organic compounds (VOCs), including ethylene [4], methyl salicylate [5], methyl jasmonate [6,7], nitric oxide [8,9], and cis-3-Hexen-1-ol [10], which upregulate pathogen-related (PR) genes [10,11,12]. The tobacco proPME protein contains a long N-terminal leader sequence with a transmembrane domain, which is important for PME delivery into the cell wall [25,26]. PME participates in cell wall biogenesis during general plant growth [27,28,29,30], nematode infection [31], and pollen tube growth [32,33,34,35]

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