Unveiling the spatial distribution of aflatoxin B1 and plant defense metabolites in maize using AP-SMALDI mass spectrometry imaging.

Abstract

To cope with the presence of unfavorable compounds, plants are capable to biotransform xenobiotics, translocate both parent compounds and metabolites, perform compartmentation and segregation at cellular or tissue level. Such a scenario also applies to mycotoxins, fungal secondary metabolites with a preeminent role in plant infection. In this work, we aimed to describe the effect of the interplay between Zea mays and aflatoxin B1 (AFB1) at the tissue and organ level. To address this challenge, we used atmospheric-pressure scanning microprobe matrix-assisted laser desorption/ionization mass spectrometry imaging (AP-SMALDI MSI) to investigate in situ and from a metabolomic standpoint the biotransformation, localization and the subsequent effects of AFB1 on primary and secondary metabolism of healthy maize plants. High spatial resolution (5 µm) provided fine localization of AFB1, which was located within the root intercellular spaces, and co-localized with its phase I metabolite aflatoxin M2. We provided a parallel visualization of maize metabolic changes, induced in different organs and tissues by an accumulation of AFB1. According to our untargeted metabolomics investigation, anthocyanin biosynthesis and chlorophyll metabolism in roots are most affected. The biosynthesis of these metabolites appears to be inhibited by the AFB1 accumulation. On the other hand, metabolites found in above-ground organs suggest that the presence of AFB1 may activate the biochemical response also in absence of an actual fungal infection; indeed several plant secondary metabolites known for their antimicrobial or antioxidant activities were localized in the outer tissues, such as phenylpropanoids, benzoxazinoid, phytohormones and lipids.