Unraveling Reciprocal Lipid-Mediated Communication between Maize Seed and Aspergillus flavus

It is generally accepted, that the reciprocal exchange of molecules between plants and fungi govern the outcome of their interaction. From a multitude of potential signals, one class of oxidized lipids (oxylipins) has taken central stage in this concept. Synthesized from enzymatic and non-enzymatic peroxidation of fatty acids, oxylipins are a large and diverse group of potent endogenous signaling molecules. Because plant and fungal oxylipins are similar biochemically and structurally, a novel hypothesis has emerged that during plant-fungal interactions, that these metabolites are exchanged, perceived, and affect the behavior of opposing partner. This study sought to explore this hypothesis and assign a role to specific oxylipin-producing enzymes from maize and Aspergillus flavus within the context of the oxylipin-mediated cross-kingdom crosstalk.

Maize wild-type and near-isogenic mutants for several lipoxygenase (LOX) and 12-oxophytodienoate reductases (OPR) related to jasmonic acid biosynthesis and nine oxylipin-mutant strains of Aspergillus flavus were utilized to investigate the contribution of oxylipins from the plant and the fungi on fungal ability to colonize the host, sporulate and produce aflatoxin. Phytohormone content and gene expression analyses of infected seed were preformed to explore potential associations of defense hormones with fungal pathogenesis processes.

Results showed that several genes involved in JA biosynthesis affect specific fungal processes. Despite belonging to separate subgroups, both LOX3 and LOX7 are involved in defense against colonization. Additionally, LOX3 expression correlates negatively with colonization and lox3 knockout mutants are more susceptible regardless of the fungal genotype indicating a general defensive role for LOX3 against A. flavus colonization. An unexpected major finding from this study is that JA biosynthesis genes appear to promote aflatoxin accumulation.

Results provide evidence that the fungal LOX gene is required for normal colonization of seed, while PpoA is required for normal conidia and aflatoxin production. The ratio of ABA/JA correlates positively with aflatoxin accumulation.

These findings are expected to expedite studies of seed-fungal interactions, lead to uncovering novel regulators of seed defense, find specific host genes and signals that regulate conidiation and mycotoxin production, and eventually provide the maize industry with genetic targets and biochemical markers for selecting aflatoxin resistant lines.