Elevated methylglyoxal levels inhibit tomato fruit ripening by preventing ethylene biosynthesis

Abstract

Methylglyoxal (MG), a toxic compound produced as a byproduct of several cellular processes, such as respiration and photosynthesis, is well known for its deleterious effects, mainly through glycation of proteins during plant stress responses. However, very little is known about its impact on fruit ripening. Here, we found that MG levels are maintained at high levels in green tomato (Solanum lycopersicum L.) fruits and decline during fruit ripening despite a respiratory burst during this transition. We demonstrate that this decline is mainly mediated through a glutathione-dependent MG detoxification pathway and primarily catalyzed by a glyoxalase I enzyme encoded by the SlGLYI4 gene. SlGLYI4 is a direct target of the MADS-box transcription factor RIPENING INHIBITOR (RIN), and its expression is induced during fruit ripening. Silencing of SlGLYI4 leads to drastic MG overaccumulation at ripening stages of transgenic fruits and interferes with the ripening process. MG most likely glycates and inhibits key enzymes such as methionine synthase and S-adenosyl methionine synthase in the ethylene biosynthesis pathway, thereby indirectly affecting fruit pigmentation and cell wall metabolism. MG overaccumulation in fruits of several non-ripening or ripening-inhibited tomato mutants suggests that the tightly regulated MG detoxification process is crucial for normal ripening progression. Our results underpin a SlGLYI4-mediated regulatory mechanism by which MG detoxification controls fruit ripening in tomato.

Decrypting Molecular Mechanisms Involved in Counteracting Copper and Nickel Toxicity in Jack Pine (Pinus banksiana) Based on Transcriptomic Analysis

“…Excess nickel induces the overproduction of MG [283]. At higher concentrations, MG can reduce photosynthesis activity, impede root growth, decrease seed germination, cause chlorosis, and prevent ethylene synthesis [284][285][286][287][288][289]. Excess MG can also be detrimental to the function of critical enzymes and proteins, as MG facilitates the glycation of arginine and lysine [290].…”

Transcriptome uncovers the key role of secondary metabolites in methylglyoxal-induced thermotolerance in maize seedlings

“…Recently, MG has been emerging as a signaling role in organism system (Hoque et al 2016;Mostofa et al 2018). In plants, MG, as a signaling molecule, takes part in the regulation of seed germination, plant growth, development, reproduction, fruit ripening, and response to biotic and abiotic stress (Mostofa et al 2018; Kim et al 2022;Liang et al 2022;Gambhir et al 2023;Lin et al 2023). In Salix matsudana Koidz.…”

Off-putting! No red, no ripe: methylglyoxal inhibits fruit ripening

“…In this issue of Plant Physiology, Gambhir et al (2023) investigated the underlying mechanism of MG detoxification through the help of glyoxalase enzymes in fruit development. To establish the role of MG in fruit ripening, they treated wild-type (WT) tomatoes with exogenous MG, which slowed down ripening compared with the control.…”

“…GLYI4 and ethylene induce the different genes related to ethylene signaling, carotenoid synthesis, and cell wall modification. The figure is adapted from Gambhir et al 2023 and created by BioRender.com.…”