Biotrophic Development of Ustilago maydis and the Response of Its Host Plant Maize

Fungal plant pathogens affect the quality of food and feed produced from infected plants and cause substantial yield losses every year. Especially fungi infecting cereal crops represent an ernormous thread. The biotrophic fungus Ustilago maydis is the causative agent of the smut disease on maize. Mo...

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Bibliographic Details
Main Author: Wahl, Ramon
Contributors: Feldbrügge, Michael (Dr.) (Thesis advisor)
Format: Dissertation
Language:English
Published: Philipps-Universität Marburg 2009
Biologie
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Summary:Fungal plant pathogens affect the quality of food and feed produced from infected plants and cause substantial yield losses every year. Especially fungi infecting cereal crops represent an ernormous thread. The biotrophic fungus Ustilago maydis is the causative agent of the smut disease on maize. Molecular pathways essential for the initiation of fungal pathogenicity, like mating of two compatible sporidia, the establishment of an infectious dikaryon and the penetration process leading to plant infection are intensively studied in U. maydis. However, the strategies used by the fungus to proliferate within the plant and to deal with the hostile environment, are vastly unknown. This dissertation investigates the complex molecular interplay between Ustilago maydis and its host plant in more detail, focusing on three different aspects. In U. maydis the initiation of sexual development and pathogenicity is controlled by two homedomain proteins bE and bW, which form an active transcription factor after fusion of two compatible sporidia. By constructing temperature-sensitive bE proteins, I was able to demonstrate that also the proliferation of U. maydis within the plant is regulated by the b mating type transcription factor (2.1). The inactivation of the bW/bE complex within the plant stops fungal development and leads to the deregulation of secreted proteins, which are believed to interfere with plant defense responses. U. maydis establishes a compatible biotrophic relationship with its host. To analyze the plant cell responses towards this forced interaction, global expression analysis and metabolic profiling were performed monitoring a time-course of infection (2.2). Expression analyses revealed an initial recognition of U. maydis by the maize plant, leading to the induction of basal plant defense responses. After U. maydis has penetrated the plant these defense responses are suppressed, suggesting an active interference with the plant immune system. Moreover, during disease progression U. maydis infected maize leaves do not develop into photosynthetically active source tissues, but maintain the characteristics of a nutrient sink. Like typical plant nutrient sinks the infected area is supplied with sucrose that is feeding the fungus. As nutrient availability determines the fitness of the pathogen, it also determines the pathogens success to conquer the plant. Thus, biotrophic fungi like U. maydis have to develop strategies to feed on nutrients provided by a living host plant. By identifying two U. maydis sugar transporters, Srt1 and Hxt1, as necessary for full fungal virulence, I was able to analyze which plant-derived carbohydrates are crucial for biotrophic development (2.3; 2.4). Srt1, a novel kind of sucrose transporter, is exclusively expressed during infection. Its unusual high sucrose affinity is well suited to compete with plant-derived sucrose uptake systems at the plant/fungus interfacen (2.3). Hxt1 utilizes hexoses glucose, fructose and mannose, and with lower affinity also galactose and xylose. Deletion of hxt1 reduces fungal pathogenicity, influences growth and hampers monosaccharide-dependent gene regulation. Moreover, expression analysis revealed that Hxt1 has a dual function as monosaccharide-transporter and -sensor (2.4). As double-deletion mutants of hxt1 and srt1 fail to induce severe disease symptoms, both uptake of sucrose and its cleavage products glucose and fructose are crucial for in planta development of U. maydis (2.4). U. maydis is recognized by the maize plant already prior to infection, resulting in the induction of basal plant defense responses. However, as soon as the fungus penetrates the plant these defense responses are manipulated by U. maydis, most probably caused by the action of fungal secreted proteins interfering with recognition and defense pathways. During disease progression, the infected maize tissue remains a sucrose-dependent nutrient sink, which lacks photosynthetic activity. This sink supplies U. maydis with sucrose and hexoses utilized by Srt1 and Hxt1 to promote fungal growth. Initiation and maintenance of the biotrophic interaction, including the expression of secreted proteins necessary to manipulate the host, are regulated by a complex transcription cascade, which is controlled by the bE/bW heterodimer. The b-cascade not only regulates fungal proliferation and differentiation, but also adapts the fungal needs towards changing plant tissues.
DOI:https://doi.org/10.17192/z2009.0479