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The autophagy genes ATG8 and ATG1 affect morphogenesis and pathogenicity in Ustilago maydis.

ABSTRACT: Autophagy is a complex degradative process in which cytosolic material, including organelles, is randomly sequestered within double-membrane vesicles termed autophagosomes. In Saccharomyces cerevisiae, the autophagy genes ATG1 and ATG8 are crucial for autophagy induction and autophagosome assembly, respectively, and their deletion has an impact on the autophagic potential of the corresponding mutant strains. We were interested in the role of autophagy in the development and virulence of U. maydis. Using a reverse genetic approach, we showed that the U. maydis ATG8 orthologue, atg8, is associated with autophagy-dependent processes. Deletion of atg8 abolished autophagosome accumulation in the vacuoles of carbon-starved cells and drastically reduced the survival of U. maydisDeltaatg8 mutant strains during these conditions. In addition, atg8 deletion had an impact on the budding process during saprobic haploid growth. The infection of maize with compatible Deltaatg8 strains resulted in fewer galled plants, and fungal gall colonization was strongly reduced, as reflected by the very low hyphal density in these tissues. Deltaatg8 infections resulted in the formation of very few teliospores. To corroborate the role of autophagy in U. maydis development, we also deleted the ATG1 orthologue, atg1. Deletion of atg1 yielded phenotypes similar to the Deltaatg8 strains during saprobic growth, but of lower magnitude. The Deltaatg1 strains were only slightly less pathogenic than the wild-type and teliospore production was not affected. Surprisingly, atg1 deletion in the Deltaatg8 background exacerbated those phenotypes already observed in the Deltaatg8 and Deltaatg1 single-mutant strains, strongly suggesting an additive phenotype. In particular, the double mutant was completely suppressed for plant gall induction.

SUBMITTER: Nadal M

PROVIDER: S-EPMC6640536 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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The autophagy genes ATG8 and ATG1 affect morphogenesis and pathogenicity in Ustilago maydis.

Nadal Marina M Gold Scott E SE

Molecular plant pathology 20100701 4

Autophagy is a complex degradative process in which cytosolic material, including organelles, is randomly sequestered within double-membrane vesicles termed autophagosomes. In Saccharomyces cerevisiae, the autophagy genes ATG1 and ATG8 are crucial for autophagy induction and autophagosome assembly, respectively, and their deletion has an impact on the autophagic potential of the corresponding mutant strains. We were interested in the role of autophagy in the development and virulence of U. maydi ...[more]

PMID: 20618705

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Project description:Ustilago maydis is a basidiomycete fungus that exhibits a yeast-like and a filamentous form. Growth of the fungus in the host leads to additional morphological transitions. The different morphologies are characterized by distinct nuclear movements. Dynein and alpha-tubulin are required for nuclear movements and for cell morphogenesis of the yeast-like form. Lis1 is a microtubule plus-end tracking protein (+TIPs) conserved in eukaryotes and required for nuclear migration and spindle positioning. Defects in nuclear migration result in altered cell fate and aberrant development in metazoans, slow growth in fungi and disease in humans (e.g. lissencephaly). Here we investigate the role of the human LIS1 homolog in U. maydis and demonstrate that it is essential for cell viability, not previously seen in other fungi. With a conditional null mutation we show that lis1 is necessary for nuclear migration in the yeast-like cell and during the dimorphic transition. Studies of asynchronous exponentially growing cells and time-lapse microscopy uncovered novel functions of lis1: It is necessary for cell morphogenesis, positioning of the septum and cell wall integrity. lis1-depleted cells exhibit altered axes of growth and loss of cell polarity leading to grossly aberrant cells with clusters of nuclei and morphologically altered buds devoid of nuclei. Altered septum positioning and cell wall deposition contribute to the aberrant morphology. lis1-depleted cells lyse, indicative of altered cell wall properties or composition. We also demonstrate, with indirect immunofluorescence to visualize tubulin, that lis1 is necessary for the normal organization of the microtubule cytoskeleton: lis1-depleted cells contain more and longer microtubules that can form coils perpendicular to the long axis of the cell. We propose that lis1 controls microtubule dynamics and thus the regulated delivery of vesicles to growth sites and other cell domains that govern nuclear movements.

Dataset Information

The autophagy genes ATG8 and ATG1 affect morphogenesis and pathogenicity in Ustilago maydis.

Publications

The autophagy genes ATG8 and ATG1 affect morphogenesis and pathogenicity in Ustilago maydis.

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