A small Ustilago maydis effector acts as a novel adhesin for hyphal aggregation in plant tumors

The biotrophic basidiomycete fungus Ustilago maydis causes smut disease in maize. Hallmarks of the disease are characteristic large tumors in which dark pigmented spores are formed. Here, we functionally characterized a novel core effector lep1 (late effector protein 1) which is highly expressed during tumor formation and contributes to virulence. We characterize lep1 mutants, localize the protein, determine phenotypic consequences upon deletion as well as constitutive expression, and analyze relationships with the repellent protein Rep1 and hydrophobins. In tumors, lep1 mutants show attenuated hyphal aggregation, fail to undergo massive late proliferation and produce only a few spores. Upon constitutive expression, cell aggregation is induced and the surface of filamentous colonies displays enhanced hydrophobicity. Lep1 is bound to the cell wall of biotrophic hyphae and associates with Rep1 when constitutively expressed in hyphae. We conclude that Lep1 acts as a novel kind of cell adhesin which functions together with other surface-active proteins to allow proliferation of diploid hyphae as well as for induction of the morphological changes associated with spore formation.

Automated summary

The novel core effector lep1 is highly expressed in maize smut disease and contributes to tumor formation and virulence. Mutants lacking lep1 show attenuated growth and spore production in tumors, while constitutive expression induces cell aggregation and enhanced hydrophobicity on the colony surface. Lep1 acts as a new kind of cell adhesin, working with other surface-active proteins to facilitate hyphal proliferation and morphological changes associated with spore formation.