Ustilago maydis, the corn smut fungus, has an unusual diploid mitotic stage

ABSTRACT

Ustilago maydis causes common smut disease in maize. Although pathogenic diploid strains of the fungus have been known for many years, the normal life cycle was thought to involve an extended dikaryotic stage, with nuclear fusion occurring in immature teliospores. However, microscopic examination of both living and fixed tumor material showed that nuclei fuse long before sporulation begins and that tumors are filled with uninucleate cells undergoing mitosis. Quantification of DNA in the nuclei confirmed these observations. Additionally, fungal cells from tumor material placed on nutrient agar produced colonies of diploid budding cells. Time-lapse observations showed that at least some of these colonies arose from thin-walled fungal cells rather than from immature spores. Ultrastructural examination of developing teliospores from tumors confirmed that they were uninucleate. Condensed chromatin and other structures characteristic of nuclei in prophase I of meiosis were observed. These observations support revising the U. maydis life cycle to include a diploid mitotic stage that corresponds with rapid tumor enlargement and conversion of plant to fungal biomass. Because mitotic division of diploid nuclei is so unusual as a life cycle feature in the fungi, it will be interesting to explore the consequences of its presence in U. maydis.

KEYWORDS:

• dikaryon
• synaptonemal complex
• zygotic meiosis

Acknowledgments

We thank G. Steinberg and R. Kahmann for U. maydis strains. Microscopy equipment was funded by several National Science Foundation grants, including DBI0821298 and MRI0115962. Several undergraduate research students were involved in preliminary studies that contributed to this work; they include Adeline Fagan, Alexa Giacobbo, and Wenlan Yu. We also thank two anonymous reviewers for helpful suggestions.

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