When a maize plant is attacked by the fungus Ustilago maydis, tumor-like tissue growths occur at the site of infection. How the pathogen causes this response in its host has long been unknown. But a University of Bonn study has now shown how the fungus takes over the plant’s function for forming lateral roots. The findings have been published in the journal New Phytologist.
Ustilago maydis attacks the leaves of the maize plant. Galls conspicuously form at the infection site, which may be as large as a child’s head. The harmful fungus benefits from this response as the massive tissue growth diverts energy and resources which are then unavailable to defend against the pathogen. Ustilago also benefits from an ideal nutrient supply found in the tissue, from which it can flourish.
“For a long time, it was not properly understood how the fungus causes its host to form galls,” says Professor Armin Djamei, head of the Department of Plant Pathology of the Institute of Crop Science and Resource Conservation (INRES) at the University of Bonn, whose research group is working to discover the mechanism. “We knew that Ustilago produces hundreds of proteins that manipulate the maize. ‘Tip effectors’ are one type of these proteins.”
Fungal genes inserted into the plant genome
The researchers inserted the fungal genes containing the instructions for forming tip effectors into the genome of the model plant Arabidopsis thaliana. The plant responded by producing proteins that are normally produced by the fungus, which made it possible to find out the precise impact of these molecules.
“Our genetically modified plants exhibited characteristic abnormalities in their roots,” relates Dr. Mamoona Khan, who conducted the experiments in large part. “There they formed ‘calli,’ i.e. tissue with fast-multiplying cells. The calli consist of plant stem cells which under normal circumstances are activated during the process of lateral root formation, so that they start to divide.” By conducting genetic experiments on maize and further analyses, the researchers were able to show that this discovery is very likely relevant to the natural host of Ustilago maydis.
Leaf pest hijacks root formation
Ustilago appears to hijack the lateral root formation function in order to accelerate cell division activity in maize leaves, leading to the formation of galls. This hypothesis is supported by additional findings by the team that tip effectors regulate the formation of various transcription factors, which help determine what genes are expressed and in what quantity.
The transcription factors that have to be upregulated for lateral roots to form are known. The researchers altered these factors in maize plants so that they no longer functioned. When infected by Ustilago, those plants only developed very small galls. “We also did a comparison against the genes that are active in gall formation and lateral root development in normal maize plants,” Khan elaborates, “and found significant similarities that cannot be merely coincidental.”
Valuable insights for breeding more resistant varieties
Ustilago maydis produces no toxins, so infected corn is still usable as animal feed without problem. The pathogen thus does not pose a major agricultural problem. In certain related species however, the situation differs. “Among the smut fungi, which include Ustilago, there are a few important pests,” points out Professor Armin Djamei, who is also active in the Sustainable Futures Transdisciplinary Research Area (TRA) and in the PhenoRob Cluster of Excellence at the University of Bonn. “Obtaining a better understanding of infection mechanisms could potentially allow breeding crop varieties that are resistant to those pathogens.”
Institutions involved and funding secured
Funding for the study was provided by the European Research Council (ERC), the Austrian Science Fund (FWF), the Austrian Academy of Sciences and the German Research Foundation (DFG).