Novel approaches to investigating Ustilago maydis pathogenesis: meiosis, phytohormones and non-coding RNAs

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Rust and smut fungi can result in losses of $100s of millions in Canada each year because they devastate crops used for food, forestry and bioenergy. Traditional research has not provided a sustainable way to control them. The new approaches in this proposal provide the potential for novel control measures that could give us the edge we need in controlling these fungi. Both smut and rust fungi must grow in a plant to reproduce, and when they grow in the plant they take their food from the plant while keeping it alive. This type of ‘eating’ by the fungus is called biotrophy. To study these fungi requires the ability to grow them in the lab and most of the rust fungi can only grow on the plant so they are difficult to work with. In contrast, some of the smut fungi, and particularly the one causing common smut of corn, can be grown in the lab and are relatively easy to study. This proposal uses the corn smut fungus to learn about how it causes disease with the idea of transferring this knowledge to the harder to study smuts and rusts. The approach of this proposal is unique as it focuses on investigating: why the smut needs to grow in the plant, what chemicals smuts produce that have a large impact on disease development and, since we know these organisms have lived with plants for a very long time, whether there is something about the very core of their life style that might influence their ability to cause disease. One thing that these organisms require plants for is sex. That means when the smut fungus infects corn it must go through a sexual cycle to cause disease and the outcome of this cycle is the production of black sooty fungal spores that spread the disease. The fact that the sexual cycle and the disease cycle occur at the same time suggests that the fungus must control its sexual reproduction at the same time that it controls its ability to cause disease. So we reasoned, that if we could understand how it controls sex then we would better understand how it controls disease. Our early investigations are promising because we identified a gene that controls sex in other organisms and found that it controls the ability to cause disease in corn smut. We are investigating the function of this gene during disease development. Our wok also revealed that the corn smut fungus makes its own version of plant hormones which it releases to change the structure and physiology of the corn plant. Corn smut disease includes the fungus causing the corn cells to divide and form a tumor in which the fungus grows, and then redirecting plant made nutrients to this tumor. Basically, the fungus tricks the plant into providing it with food and a place to live. We are working on understanding how and when the smut makes plant hormones, and also on how the fungal plant hormones change the plant. Finally we discovered something quite different when we were investigating the sequence of this organism’s genome. If you consider the genome the library of the cell and the genes are the books, the way the genome works is you copy the book to take it away. We discovered that many times two different copies of the book are made and that the two copies can stick together (these two copies represent the sense and antisense RNAs). It turns out that producing the second copy of the gene is used to control the reading of the first copy and we have learned that this control might be how the organisms determine if it will cause disease. Our investigations will test this idea. The results of the proposed research will increase our understanding of how fungi infect plants. This will allow us to devise novel ways to fight the smut and rust fungi, providing new tools in our battle to reduce disease, and giving us a more stable food supply.