Metabolomics links induced responses to the wheat pathogen – tan spot – (Pyrenophora tritici-repentis) to the biosynthesis of flavonoids and bioenergetic metabolism

Abstract

Abstract Introduction Tan Spot disease of wheat is caused by Pyrenophora tritici-repentis (Ptr), and most of the yield loss is attributed to diseased flag leaves. Few sources of Ptr-resistant germplasm have been established so the responses of wheat to Ptr require further elucidation. Objectives The study aimed to characterise the flag-leaf metabolomes of two spring wheat cultivars (Triticum aestivum L. cv. PF 080719 [PF] and cv. Fundacep Horizonte [FH]) in response to Pyrenophora tritici-repentis infection to gain insights into pathogenicity and defence mechanisms associated with the Tan Spot disease. Methods PF and FH plants were inoculated with a Ptr strain that produces the necrotrophic toxin ToxA. The metabolic scenarios in flag leaves prior to (0 h) and during (24, 48, 72, and 96 h post-inoculation [hpi]) challenge with Ptr were investigated using untargeted flow infusion ionisation – high resolution mass spectroscopy (FIE-HRMS). Results At the flag-leaf stage, both cultivars displayed susceptibility to Ptr. Comparisons of Ptr- and mock-inoculated plants indicate a major metabolic shift occurred at 24 hpi in FH, and at 48 hpi in PF. In PF, there was a significant accumulation of flavonoids, phenylpropanoids, and glucosinolates. Pathway enrichment analysis suggested that Ptr-triggered alterations in chloroplast and photosynthetic machinery in both cultivars, especially in FH at 96 hpi. In PF, alterations in sugar metabolism as well as in glycolysis and glucogenesis pathways were observed. In a wheat-Ptr interactome in integrative network analysis, the pathways “flavone and flavonol biosynthesis” and “starch and sucrose metabolism” were the key metabolic processes underlying PF-FH-Ptr interactions. Conclusion These observations suggest the potential importance of flavone and flavonol biosynthesis as well as bioenergetic shifts in susceptibility to Ptr. Further, they highlight the applicability of metabolomics to provide novel insights into wheat pathosystems.