Carbon acquisition during pathogenic development of Ustilago maydis and Colletotrichum graminicola
Plant Breeding and Plant Pathology
Final Report Abstract
Biotrophic fungi depend on living host tissue for development. The biotrophic life style ensures a sustainable supply of nutrients, but also requires a high degree of specialization and adaptation to the host. During the last funding period, we have focused on the utilization of carbohydrates by the corn smut fungus Ustilago maydis with major impact during both biotrophic and the saprotrophic life phase We have shown previously that in addition to the sucrose transporter Srt1 also the hexose transporter Hxt1 is required for pathogenic development of U. maydis in maize seedlings. We have extended the studies and show that the carbohydrate acquisition strategies of U. maydis do not differ significantly in sink and source tissues or different plant organs. We have identified three plant sugar efflux transporters the SWEET family whose expression is induced during the biotrophic interaction, two of which transport glucose, while the third serves as a sucrose carrier. The identified transporters could potentially pose as the counterpart to the fungal glucose and sucrose transporters, Hxt1 and Srt1, ensuring the supply for U. maydis hyphae with glucose and sucrose from the cytoplasm of the surrounding host cells during the biotrophic phase. Deletion of hxt1 was shown to lead to enhanced growth on galactose-containing media, which was interpreted as a potential sensor function of Hxt1. We show now that galactose has a toxic effect on U. maydis, which is favored by Hxt1-dependent galactose transport. The toxic effect of galactose on U. maydis was supported by the identification of a mutant in gal1 (encoding galactokinase) with increased galactose tolerance. The reduced activity results in lower levels of the toxic product of the galactokinase, galactose-1-phosphate (gal-1-P). However, additional mechanisms for the toxicity of galactose must exist, as (1) mutants deleted for gal1 are still incapable to grow on media with galactose, and (b) the identified gal1 mutant allele is dominant to the wildtype allele. In humans, mutations in gal1 lead to disorders with severe symptoms, as, for example, cataracts. As both proteins and gene regulation of genes resemble much more the situation in U. maydis than in S. cerevisiae, future studies on the Gal metabolism are expected also to have impact on the so far not well understood effects of the Gal1 mutations in the human system. A sensor function of Hxt1 during pathogenic development was supported by the isolation of different hxt1 mutant alleles that, upon ectopic expression, lead, in contrast to the deletion, to a complete loss of pathogenic development. Microarray analysis during the initial stages of development indicate an alteration of glucose dependent gene expression in the fungal cells, which may interfere with the nutritional adaptation of the fungus at the switch from saprophytic to biotrophic growth.
Publications
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(2010) A model of Ustilago maydis leaf tumor metabolism. Plant Signal Behav 5: 1446-1449
Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, et al.
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(2010) A novel high-affinity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol 8: e1000303
Wahl R, Wippel K, Goos S, Kämper J, Sauer N
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(2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant physiology 152: 293-308
Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, et al.
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(2011) Common Motifs in the Response of Cereal Primary Metabolism to Fungal Pathogens are not Based on Similar Transcriptional Reprogramming. Front Plant Sci 2: 39
Voll LM, Horst RJ, Voitsik AM, Zajic D, Samans B, et al.
