Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/23/2021
Publication Date: 6/24/2021
Citation: Y-S. Park; E.J. Borrego; X. Gao, S.A. Christensen; E. Schmelz; A. Lanubile; D.A. Drab; W. Cody; H. Yan; W-B. Shim; M.V. Kolomiets. 2021. Fusarium verticillioides induces maize-derived ethylene to promote virulence by engaging fungal G-protein signaling. Molecular Plant Microbe Interactions https//doi.org/10.1094/MPMI-09-20-0250-R
DOI: https://doi.org/10.1094/MPMI-09-20-0250-R

Interpretive Summary: Pathogens that cause harmful crop diseases are mitigated by small molecules that regulate plant defense. As such, the volatile ethylene has been broadly characterized as a defensive hormone against fungal pathogens. However, while studying Fusarium ear rot caused by Fusarium verticillioides, scientists at the USDA-ARS Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, in conjunction with researchers from Texas A&M University, discovered that ethylene and its regulatory pathways can be hijacked by fungal pathogens to make plants more susceptible to Fusarium ear rot. These results demonstrate that pathogens can evolve to manipulate specialized roles in plant defense. Findings from this study will provide breeders with useful molecular tools to develop new corn varieties with enhanced protection against mycotoxigenic fungi like F. verticillioides.

Technical Abstract: Seed contamination with Fusarium-produced fumonisin is a major limiting factor for maize production. Meta-analyses of QTLs for Fusarium ear rot resistance uncovered several ethylene (ET) biosynthesis and signaling genes within them, implicating ET in maize interactions with F. verticillioides. We tested this hypothesis using knock-out mutants of the 1-aminocyclopropane-1-carboxylate (ACC) synthases, ZmACS2 and ZmACS6. Infected wild-type (WT) seed emitted five-fold higher ET levels compared to controls, whereas ET was significantly reduced in the acs2 and acs6 single and double mutants. The mutants supported reduced fungal biomass, conidia and fumonisin content. Normal virulence was restored in the acs6 mutant by exogenous treatment with ET precursor, ACC. Secondary metabolite analysis uncovered mis-regulation of the production of auxin and nerolidol in the acs2 acs6 double mutants. Exogenous auxin promoted virulence, whereas nerolidol contributed to resistance. We show that fungal G-protein signaling is required for virulence via induction of ET. F. verticillioides Gß subunit and two regulators of G-protein signaling mutants displayed reduced seed colonization and decreased ET levels. This defect was rescued by exogenous ACC. We conclude that pathogen-induced ET facilitates F. verticillioides colonization of seed, and that host ET production is manipulated via G-protein signaling of F. verticillioides to facilitate disease.