Isha Mittal 1, Syeda Alam 1, Elena Shulaev 1, Katherine Berg 2, Yanhong Dong 3, Harold N. Trick 4, Michael Kolomiets 2, Steve Scofield 5, Jyoti Shah 1
1. University of North Texas, Department of Biological Sciences and BioDiscovery Institute, Denton, Texas
2. Texas A&M University, Department of Plant Pathology and Microbiology, College Station, Texas
3. University of Minnesota, Department of Plant Pathology, St. Paul, Minnesota
4. Kansas State University, Department of Plant Pathology, Manhattan, Kansas
5. USDA-Agricultural Research Service, West Lafayette, Indiana
Corresponding author: Jyoti Shah, Jyoti.Shah@unt.edu
Mittal, Isha
Fusarium head blight (FHB), caused by Fusarium graminearum (Fg), is a major disease that threatens global wheat production by reducing grain yield and contaminating grain with trichothecene mycotoxins. While fungicides are widely used for disease management, their effectiveness is limited, and their use raises environmental concerns. Therefore, identifying host genes that influence FHB susceptibility or resistance is critical for developing sustainable control strategies. Oxylipins, lipid-derived signaling molecules produced by both plants and fungi, play multifaceted roles in defense and inter-kingdom communication. Our research identified the a oxylipin synthesizing 9-lipoxygenase, Lpx3, as a susceptibility factor in wheat interaction with Fg. Lpx3 knockdown enhanced resistance to Fg and significantly
reduced mycotoxin accumulation compared to the wild type. To elucidate the molecular mechanisms underlying this enhanced resistance, dual RNA sequencing of wheat and the pathogen was conducted using spikelets collected from mock- and Fg-inoculated wild type and Lpx3RNAi lines at 24 and72 hours post-inoculation. Comparative transcriptomic analyses revealed that Lpx3 knockdown led to differential regulation of host genes associated with fatty acid metabolism, plant hormone signaling, and defense-related secondary metabolism. Among the most highly induced pathways was flavonoid biosynthesis, including strong upregulation of chalcone synthase (CHS) genes. Given
the known antimicrobial and signaling roles of flavonoids, these results suggested a link between oxylipin metabolism and secondary metabolite-mediated defense. To explore this relationship, we examined Arabidopsis thaliana
mutants deficient in CHS (tt4). These mutants displayed enhanced susceptibility to Fg, providing functional evidence that flavonoid biosynthesis contributes to floral defense. On the fungal side, several virulence and pathogenicity associated genes, including those encoding effector proteins and detoxification enzymes, exhibited altered expressions in the Lpx3RNAi line. Together, these findings reveal that suppression of a single host lipoxygenase gene can reprogram both lipid and flavonoid derived defense networks and modulate fungal pathogenic responses, likely through cross-kingdom lipid and secondary metabolite signaling. Overall, our results highlight Lpx3 and CHS as key molecular players influencing FHB outcome and demonstrate the potential of targeting oxylipin flavonoid crosstalk to develop wheat cultivars with durable resistance to Fg.
Acknowledgements: This work was supported by the USDA-NIFA (Award 2021-67013-33573), and at various stages by USDA (Agreements 59-0206-7-006, 59-0206-0-186, 59-0206-0-179, 59-0206-0-151, 59-206-2-161) as cooperative projects with the USWBSI, and Agreement 58-5020-1-013 as a USDA-ARS NACA. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the USDA.
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