The Multifunctional β-Oxidation Enzyme Is Required for Full Symptom Development by the Biotrophic Maize Pathogen Ustilago maydis

Abstract

The transition from yeast-like to filamentous growth in the biotrophic fungal phytopathogen Ustilago maydis is a crucial event for pathogenesis. Previously, we showed that fatty acids induce filamentation in U. maydis and that the resulting hyphal cells resemble the infectious filaments observed in planta. To explore the potential metabolic role of lipids in the morphological transition and in pathogenic development in host tissue, we deleted the mfe2 gene encoding the multifunctional enzyme that catalyzes the second and third reactions in ␤-oxidation of fatty acids in peroxisomes. The growth of the strains defective in mfe2 was attenuated on long-chain fatty acids and abolished on very-long-chain fatty acids. The mfe2 gene was not generally required for the production of filaments during mating in vitro, but loss of the gene blocked extensive proliferation of fungal filaments in planta. Consistent with this observation, mfe2 mutants exhibited significantly reduced virulence in that only 27% of infected seedlings produced tumors compared to 88% tumor production upon infection by wild-type strains. Similarly, a defect in virulence was observed in developing ears upon infection of mature maize plants. Specifically, the absence of the mfe2 gene delayed the development of teliospores within mature tumor tissue. Overall, these results indicate that the ability to utilize host lipids contributes to the pathogenic development of U. maydis.

Peroxisomal and Mitochondrial β-Oxidation Pathways Influence the Virulence of the Pathogenic Fungus Cryptococcus neoformans

“…Defects in ␤-oxidation compromise virulence in phytopathogenic fungi (2,31,32,61,81; see also the accompanying article by Kretschmer et al [33a]). For example, we previously demonstrated that a mutant lacking the multifunctional enzyme Mfe2 in the basidiomycete Ustilago maydis had reduced virulence and sporulation on maize (32).…”

“…Defects in ␤-oxidation compromise virulence in phytopathogenic fungi (2,31,32,61,81; see also the accompanying article by Kretschmer et al [33a]). For example, we previously demonstrated that a mutant lacking the multifunctional enzyme Mfe2 in the basidiomycete Ustilago maydis had reduced virulence and sporulation on maize (32). In addition, the loss of ␤-oxidation in the human pathogen Candida albicans slightly attenuates virulence, although this fungus has only the peroxisomal pathway (55,56,59,60).…”

“…This adaptation may also be important for interactions with macrophages in mammalian hosts, where the fungus may encounter lipids as signals or carbon sources. For U. maydis, fatty acids also act as signaling molecules that trigger the transition from yeast to filamentous growth that is important for plant infection, and peroxisomal ␤-oxidation contributes to this activity (32). In contrast, C. neoformans does not respond to fatty acids with filamentous growth, although oleic acid appears to be a growth factor.…”

Defects in Mitochondrial and Peroxisomal β-Oxidation Influence Virulence in the Maize Pathogen Ustilago maydis

“…The invasive filaments proliferate in the plant and ultimately incite large tumors that fill with black teliospores (2). In addition to mating, the switch from yeast-like to filamentous growth is triggered by low pH, low nitrogen, phosphate, and fatty acids (5,27,28,34,49). Recently, we showed that the morphological switch in response to specific fatty acids is influenced by peroxisomal ␤-oxidation, thus raising the possibility that this process is important for the pathogenicity of U. maydis (28).…”

“…For U. maydis, we previously found that deletion of the gene encoding the peroxisomal multifunctional enzyme (Mfe2) reduced growth on long-chain fatty acids and attenuated symptom development and teliospore formation on maize (28). Defects in ␤-oxidation are known to influence virulence in other phytopathogenic fungi.…”