Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis

Abstract

Ustilago maydis is a dimorphic fungus with a yeast-like non-pathogenic form and a filamentous (hyphal) pathogenic form that induces tumor formation in maize. Within mature tumors, hyphae give rise to teliospores, which are round, diploid cells surrounded by a specialized cell wall. Here we describe the time course of fungal development in the plant with a focus on the morphological changes in the hyphae and the pathway of teliospore formation. We confirm and extend earlier observations that U. maydis hyphae branch extensively on the leaf surface and intracellularly before induction of tumors. We observe that at later stages the filaments undergo a series of discrete morphogenetic changes leading to teliospore formation. In particular, we show that the hyphae become embedded in a mucilaginous matrix within the tumor cells and the hyphal tips become modified. The hyphae then undergo fragmentation to release individual cells that exhibit a variety of shapes on their way to becoming rounded. Finally, a specialized cell wall is deposited. Support for the existence of such a pathway comes from analysis of a mutant defective in the fuz1 gene: inactivation of fuz1 blocks production of the mucilaginous matrix and fragmentation of the hyphae, leading to a defect in teliospore formation. The different morphological changes that occur while in the plant but not in culture suggest that plant inputs play a key role in fungal development.