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The basidiomycete  Ustilago maydis  causes smut disease in maize. Colonization of the host plant is initiated by direct penetration of cuticle and cell wall of maize epidermis cells. The invading hyphae are surrounded by the plant plasma membrane and proliferate within the plant tissue. We identified a novel secreted protein, termed Pep1, that is essential for penetration. Disruption mutants of  pep1  are not affected in saprophytic growth and develop normal infection structures. However,  Δpep1  mutants arrest during penetration of the epidermal cell and elicit a strong plant defense response. Using Affymetrix maize arrays, we identified 116 plant genes which are differentially regulated in  Δpep1  compared to wild type infections. Most of these genes are related to plant defense. By  in vivo  immunolocalization, live-cell imaging and plasmolysis approaches, we detected Pep1 in the apoplastic space as well as its accumulation at sites of cell-to-cell passages. Site-directed mutagenesis identified two of the four cysteine residues in Pep1 as essential for function, suggesting that the formation of disulfide bridges is crucial for proper protein folding. The barley covered smut fungus  Ustilago hordei  contains an ortholog of  pep1  which is needed for penetration of barley and which is able to complement the  U. maydis Δpep1  mutant. Based on these results, we conclude that Pep1 has a conserved function essential for establishing compatibility that is not restricted to the  U. maydis  / maize interaction.

Pep1, a Secreted Effector Protein of Ustilago maydis, Is Required for Successful Invasion of Plant Cells