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First published online April 10, 2009; 10.1105/tpc.109.210413

The Plant Cell 21:1030

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IN BRIEF

Pexophagy in Fungal Pathogenesis

Gregory Bertoni

Science Editor

gbertoni{at}aspb.org

Autophagy is a process of cellular self-eating in which individual protein molecules, regions of cytoplasm, or entire organelles are surrounded by an autophagic membrane and delivered to the lysosome (or yeast vacuole) for degradation. It appears to occur in all eukaryotic cells and has a number of purposes: recycling of nutrients during starvation, disposal of unneeded or damaged organelles, remodeling of cell contents and structures during development or apoptosis, and defense against pathogens (Mizushima and Klionsky, 2007Go; Pollack et al., 2009Go).

A type of selective autophagy known as pexophagy involves the preferential destruction of peroxisomes (Farré and Subramani, 2004Go) and has been studied extensively in the yeast Pichia pastoris during metabolic shifts induced by altering its in vitro carbon source. The role of peroxisome function and pexophagy in phytopathogenicity is not well established, but it was recently shown that autophagic programmed cell death in the rice blast fungus Magnaporthe oryzae is necessary for fungal pathogenicity (Veneault-Fourrey et al., 2006Go). Additionally, the peroxisomal biosynthesis protein Pex6 is required for pathogenicity in both M. oryzae and Colletotrichum orbiculare, the fungal pathogen causing cucumber anthracnose.

Now, a connection between pexophagy and plant tissue invasion by fungal pathogens is reported by Asakura et al. (pages 1291–1304). By screening a random insertional mutant library of C. orbiculare for mutants defective in pathogenicity on cucumber leaves, the authors isolated a mutant with reduced virulence. The disrupted gene showed homology to P. pastoris ATG26, which encodes a sterol glucosyltransferase that activates pexophagy. The conidia of the C. orbiculare atg26 mutant germinate on leaf surfaces to produce functionally competent appressoria but are defective in their subsequent ability to form infectious hyphae (see figure ). When inoculated directly into wounds, the atg26 mutant is able to grow in host tissue, confirming a specific defect in initial host invasion.


Figure 1
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  		Appressoria (a) of wild-type C. orbiculare (left panel) produce numerous infectious hyphae (ih; stained blue), while those of the pexophagy-deficient atg26 mutant (right panel) produce very few. Bar = 10 µm.

 
Using GFP fused with the SKL peroxisomal targeting signal to monitor peroxisome synthesis and degradation, the authors show that both the wild-type and atg26 mutant strains produce numerous peroxisomes in conidia and appressoria a few hours after germination, demonstrating normal peroxisome biogenesis in the absence of the Atg26 protein. However, after 24 h, peroxisomes were degraded in vacuoles of wild-type appressoria, while those of atg26 remained. No changes in mitochondrial numbers were observed in wild-type cells, suggesting that peroxisomes are preferentially degraded during the infection process.

The authors show that the both the phosphoinositide binding domain and the catalytic domain of Atg26 are required for pexophagy and pathogenicity. Cellular localization experiments suggested that the phosphoinositide binding domain of Atg26 is required for the proper intracellular recruitment of Atg26 to membrane structures for pexophagy. They propose a model describing a potential link between peroxisome homeostasis and infection-related morphogenesis. Future studies with these and related atg mutants should provide insight into the roles of organellar dynamics in cellular differentiation and pathogenicity.

Footnotes

www.plantcell.org/cgi/doi/10.1105/tpc.109.210413

REFERENCES

Asakura, M., Ninomiya, S., Sugimoto, M., Oku, M., Yamashita, S., Okuno, T., Sakai, Y., and Takano, Y. (2009). Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell 21: 1291–1304.[Abstract/Free Full Text]

Farré, J.-C., and Subramani, S. (2004). Peroxisome turnover by micropexography: An autophagy-related process. Trends Cell Biol. 14: 515–523.[CrossRef][Web of Science][Medline]

Mizushima, N., and Klionsky, D.J. (2007). Protein turnover via autophagy: Implications for metabolism. Annu. Rev. Nutr. 27: 19–40.[CrossRef][Medline]

Pollack, J.K., Harris, S.D., and Marten, M.R. (2009). Autophagy in filamentous fungi. Fungal Genet. Biol. 46: 1–8.[CrossRef][Web of Science][Medline]

Veneault-Fourrey, C., Barooah, M., Egan, M., Wakley, G., and Talbot, N.J. (2006). Autophagic fungal cell death is necessary for infection by the rice blast fungus. Science 312: 580–583.[Abstract/Free Full Text]


Related articles in Plant Cell:

Atg26-Mediated Pexophagy Is Required for Host Invasion by the Plant Pathogenic Fungus Colletotrichum orbiculare
Makoto Asakura, Sachiko Ninomiya, Miki Sugimoto, Masahide Oku, Shun-ichi Yamashita, Tetsuro Okuno, Yasuyoshi Sakai, and Yoshitaka Takano
Plant Cell 2009 21: 1291-1304. [Abstract] [Full Text]  




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