Ustilago maydis reprograms cell proliferation in maize anthers

Abstract

The basidiomycete Ustilago maydis is a ubiquitous pathogen of maize (Zea mays), one of the world's most important cereal crops. Infection by this smut fungus triggers tumor formation in aerial plant parts within which the fungus sporulates. Using confocal microscopy to track U.maydis infection on corn anthers for 7days post-injection, we found that U.maydis is located on the epidermis during the first 2days, and has reached all anther lobe cell types by 3days post-injection. Fungal infection alters cell-fate specification events, cell division patterns, host cell expansion and host cell senescence, depending on the developmental stage and cell type. Fungal effects on tassel and plant growth were also quantified. Transcriptome profiling using a dual organism microarray identified thousands of anther genes affected by fungal infection at 3days post-injection during the cell-fate specification and rapid cell proliferation phases of anther development. In total, 4147 (17%) of anther-expressed genes were altered by infection, 2018 fungal genes were expressed in anthers, and 206 fungal secretome genes may be anther-specific. The results confirm that U.maydis deploys distinct genes to cause disease in specific maize organs, and suggest mechanisms by which the host plant is manipulated to generate a tumor.