A secondary function of trehalose-6-phosphate synthase is required for resistance to oxidative and desiccation stress in Fusarium verticillioides

Authors: MCMILLAN, SARAH - Bradley University; OBERLIE, NICOLE - Bradley University; HARDTKE, HALEY - Bradley University; MONTES, MIAH - Bradley University; Brown, Daren; MCQUADE, KRISTI - Bradley University

Submitted to: Fungal Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/20/2023
Publication Date: 1/21/2023
Citation: McMillan, S.D., Oberlie, N.R., Hardtke, H.A., Montes, M.M., Brown, D.W., McQuade, K.L. 2023. A secondary function of trehalose-6-phosphate synthase is required for resistance to oxidative and desiccation stress in Fusarium verticillioides. Fungal Biology. 127(3):918-926. https://doi.org/10.1016/j.funbio.2023.01.006.
DOI: https://doi.org/10.1016/j.funbio.2023.01.006

Interpretive Summary: The fungus Fusarium verticillioides infects corn and contaminates corn and corn products with hazardous toxins called fumonisins. Understanding how this fungus bypasses plant defenses and how these defenses impact the ability of Fusarium to make fumonisins could provide new targets to limit fungal growth and toxin contamination. Trehalose is a sugar that protects fungi from stress. Mutants of F. verticillioides, defective in an enzyme that makes trehalose, cannot cause corn disease nor make fumonisins. Researchers at Bradley University in Peoria, Illinois, in collaboration with an ARS researcher in Peoria, Illinois, found that mutants with a modified trehalose enzyme had improved ability to protect itself from stress conditions without restoring trehalose synthesis. The research identified a protective secondary function of the trehalose enzyme. These results provide a new approach to identify critical fungal protective control points and will be used by plant pathologists and other researchers to develop novel strategies to limit or control toxin contamination of grain to keep our food supply safe.

Technical Abstract: The disaccharide trehalose has long been recognized for its role as a stress solute, but in recent years some of the protective effects previously ascribed to trehalose have been suggested to arise from a function of the trehalose biosynthesis enzyme trehalose-6-phosphate (T6P) synthase that is distinct from its catalytic activity. In this paper, we use the maize pathogenic fungus Fusarium verticillioides as a model to explore the relative contributions of trehalose itself and a putative secondary function of T6P synthase in protection against stress as well as to understand why, as shown in a previous study, deletion of the TPS1 gene coding for T6P synthase reduces pathogenicity against maize. We report that the TPS1-deletion mutant of F. verticillioides is compromised in its ability to withstand exposure to oxidative stress meant to simulate the oxidative burst phase of maize defense and experiences more ROS-induced lipid damage than the wild-type strain. Eliminating T6P synthase expression also reduces resistance to desiccation, but not resistance to phenolic acids. Expression of catalytically-inactive T6P synthase in the TPS1-deletion mutant leads to a partial rescue of the oxidative and desiccation stress-sensitive phenotypes, suggesting the importance of a T6P synthase function that is independent of its role in trehalose synthesis.