Histology-guided high-resolution AP-SMALDI mass spectrometry imaging of wheat-Fusarium graminearum interaction at the root–shoot junction

Abstract

BackgroundFungal pathogens like Fusarium graminearum can cause severe yield losses and mycotoxin contamination of food and feed worldwide. We recently showed its ability to systemically colonize wheat via root infection. However, the molecular response of wheat to Fusarium root rot (FRR) infection and systemic spread is still unknown. As a molecular camera, mass spectrometry (MS) imaging combines label-free and multiplex metabolite profiling with histopathology.ResultsAtmospheric-pressure (AP)-SMALDI-MS imaging was combined with optical microscopy to study wheat-F. graminearum interaction at the root–shoot junction, which is a crucial line of defense against a pathogen that can invade all distal plant parts. To scope the functional, temporal and local aspects of FRR disease spread, metabolic changes were simultaneous visualized in diseased and healthy stem bases of the resistant cultivar Florence-Aurore at 10, 14 and 21 days after root inoculation. Histological information was used to identify disease relevant tissues and to assist the interpretation of molecular images. Detected mycotoxin compounds secreted by F. graminearum showed a route of stem infection that was consistent with observations made by microscopy. The outer epidermis and vasculature of leaf sheath were, at different disease stages, identified as prominent sites of pathogen migration and wheat protection. Wheat metabolites mapped to these relatively small tissues indicated cell wall strengthening and antifungal activity as direct defenses as well as conservation in the wheat reactions to F. graminearum diseases that affect different plant organs.ConclusionsAP-SMALDI-MS imaging at high spatial resolution is a versatile technique that can be applied to basic and applied aspects of agricultural research. Combining the technology with optical microscopy was found to be a powerful tool to gain in-depth information on almost unknown crop disease. Moreover, the approach allowed studying metabolism at the host–pathogen interface. The results provide important hints to an understanding of the complex spatio-temporal organization of plant resistance. Defense-on-demand responses to pathogen ingress were found, which provide opportunities for future research towards an improved resistance that does not negatively impact yield development in the field by saving plant resources and, moreover, may control different Fusarium diseases.Electronic supplementary materialThe online version of this article (10.1186/s13007-018-0368-6) contains supplementary material, which is available to authorized users.

Bioinformatic analysis deciphers the molecular toolbox in the endophytic/pathogenic behavior inF. oxysporumf. sp.vanillae-V. planifoliaJacks interaction

“…In the present work we found the presence at 2 dpi of genes related to the glycerophospholipid metabolism pathway, as widely reported previously (van Aarle and Olsson, 2003; Bhandari et al, 2018; Zhang et al, 2020), such as: ethanolamine kinase, acetyltransferase, phosphatidylserine decarboxylase, phosphatidylserine decarboxylase, lysophospholipase NTE1, CDP-diacylglycerol-inositol 3-phosphatidyltransferase, ethanolamine-phosphate cytidylyltransferase, and NTE family protein. Joshi and Mathur in 1987 mentioned that Fox synthesizes up to 26.4% lipids in minimal medium, being glycerophospholipids and triacylglycerols, the latter predominating.…”

Molecular mapping of qBK1Z, a major QTL for bakanae disease resistance in rice

“…It was reported that successful infection of Fusarium species is a complex process that includes adhesion, penetration (through wounds, seeds, stomatal pores) and subsequent colonization within and between cells [34,35]. Consistent with previous reports [36,37], F. fujikuroi isolate CF283 was extensively observed on the aerenchyma, pith, cortex and vascular bundle of both leaf and stem in susceptible Ilpum, whereas this was rarely observed in resistant Zenith.…”

Spermidine and other functional phytochemicals in soybean seeds: Spatial distribution as visualized by mass spectrometry imaging

“…Besides animal and human tissue analysis, MS imaging has also been adapted to insect and plant tissues (Bhandari, Schott, Römpp, Vilcinskas, & Spengler, 2015;Bhandari, Wang, et al, 2015;Dong et al, 2016). Successful applications of MS imaging include licorice rhizome imaging of flavonoids or saponins (Li, Bhandari, Janfelt, Römpp, & Spengler, 2014), metabolites in maturing and germinating oilseed rape seeds, different tissues in wheat plants, and metabolites illustrating the infection of bread wheat seeds as well as stems with the Fusarium graminearum head blight disease (Bhandari, Wang, et al, 2015;Bhandari et al, 2018). Successful applications of MS imaging include licorice rhizome imaging of flavonoids or saponins (Li, Bhandari, Janfelt, Römpp, & Spengler, 2014), metabolites in maturing and germinating oilseed rape seeds, different tissues in wheat plants, and metabolites illustrating the infection of bread wheat seeds as well as stems with the Fusarium graminearum head blight disease (Bhandari, Wang, et al, 2015;Bhandari et al, 2018).…”