Sphingolipid Effects on the Plasma Membrane Produced by Addition of Fumonisin B1 to Maize Embryos

Abstract

Fumonisin B1 is a mycotoxin produced by Fusarium verticillioides that modifies the membrane properties from animal cells and inhibits complex sphingolipids synthesis through the inhibition of ceramide synthase. The aim of this work was to determine the effect of Fumonisin B1 on the plant plasma membrane when the mycotoxin was added to germinating maize embryos. Fumonisin B1 addition to the embryos diminished plasma membrane fluidity, increased electrolyte leakage, caused a 7-fold increase of sphinganine and a small decrease in glucosylceramide in the plasma membrane, without affecting phytosphingosine levels or fatty acid composition. A 20%–30% inhibition of the plasma membrane H+-ATPase activity was observed when embryos were germinated in the presence of the mycotoxin. Such inhibition was only associated to the decrease in glucosylceramide and the addition of exogenous ceramide to the embryos relieved the inhibition of Fumonisin B1. These results indicate that exposure of the maize embryos for 24 h to Fumonisin B1 allowed the mycotoxin to target ceramide synthase at the endoplasmic reticulum, eliciting an imbalance of endogenous sphingolipids. The latter disrupted membrane properties and inhibited the plasma membrane H+-ATPase activity. Altogether, these results illustrate the mode of action of the pathogen and a plant defense strategy.

A critical review on natural compounds interacting with the plant plasma membrane H+‐ATPase and their potential as biologicals in agriculture

“…FB 1 also acts as a sphingolipid by becoming inserted into membranes due to its amphipathic nature, thereby decreasing membrane fluidity (Figure 5E) (Mahfoud et al, 2002; Gutierrez‐Najera et al, 2005). In vivo treatment of maize embryos with FB 1 indicated that the toxin first inhibits the ceramide synthase, and this action will subsequently accumulate sphinganine in the PM, changing the fluidity and thereby inhibiting PM H + ‐ATPase activity (Gutierrez‐Najera et al, 2020). The toxin must therefore have multiple functions since it changed the activity of the pump differently in vitro compared to in vivo .…”

“…Fumonisin B 1 Fumonisin B 1 (FB 1 ) is produced by various Fusarium species (Table 2, Figure 3) that cause root, stalk, and ear rot in maize (Z. mays) (Leslie, 1996). FB 1 potentially inhibits the activity of membrane-localized enzymes, such as the sphinganine Nacyltransferase, as FB 1 treatment led to the accumulation of sphinganine in the PM (Abbas et al, 1994;Gutierrez-Najera et al, 2020). The inhibitory effect of FB 1 on maize PM H + -ATPases has also been investigated (Gutierrez-Najera et al, 2005).…”

The in vitro Production Potentialities of Secondary Toxic Metabolites by the Fungal Factory Fusarium verticillioides Is, Fortunately, Largely Underestimated in Fields: Pioneering Study on Fumonisins

“…It is well known that FB1 modifies the "SphingoLipid rheostat. " Sphingolipids, such as Cer and S1P, facilitate EV biogenesis, promoting vesicle buddings inside MVB and ectosomes (Nora et al, 2020). Our TEM results demonstrate the existence of both types of EV.…”

“…Our TEM results demonstrate the existence of both types of EV. EV is known as cell-to-cell communication mediators due to their ability to transfer biomolecules among cells and to influence the extracellular microenvironment via regulation of critical nutrients (Nora et al, 2020). F. verticillioides needs to be considered as a producing ready-to-use SM factory and could be interpreted as an armed soldier, ready to shoot for maintaining its species survival.…”

“…Little is known on the possible role of these fumonisins in plants. FB1 could decrease plasmalemma fluidity (Nora et al, 2020) and produces chloroplast integrity loss (Scala et al, 2013;Xing et al, 2013;Santiago et al, 2020).…”