Blistering1 modulates penicillium expansum virulence via vesicle-mediated protein secretion

Wayne M. Jurick, Hui Peng, Hunter S. Beard, Wesley M. Garrett, Franz J. Lichtner, Dianiris Luciano-Rosario, Otilia Macarisin, Yingjian Liu, Kari A. Peter, Verneta L. Gaskins, Tianbao Yang, Joseph Mowery, Gary Bauchan, Nancy P. Keller, Bret Cooper

Research output: Contribution to journalArticle

Abstract

The blue mold fungus, Penicillium expansum, is a postharvest apple pathogen that contributes to food waste by rotting fruit and by producing harmful mycotoxins (e.g. patulin). To identify genes controlling pathogen virulence, a random T-DNA insertional library was created from wild-type P. expansum strain R19. One transformant, T625, had reduced virulence in apples, blistered mycelial hyphae, and a T-DNA insertion that abolished transcription of the single copy locus in which it was inserted. The gene, Blistering1, encodes a protein with a DnaJ domain, but otherwise has little homology outside the Aspergillaceae, a family of fungi known for producing antibiotics, mycotoxins, and cheese. Because protein secretion is critical for these processes and for host infection, mass spectrometry was used to monitor proteins secreted into liquid media during fungal growth. T625 failed to secrete a set of enzymes that degrade plant cell walls, along with ones that synthesize the three final biosynthetic steps of patulin. Consequently, the culture broth of T625 had significantly reduced capacity to degrade apple tissue and contained 30 times less patulin. Quantitative mass spectrometry of 3,282 mycelial proteins revealed that T625 had altered cellular networks controlling protein processing in the endoplasmic reticulum, protein export, vesicle-mediated transport, and endocytosis. T625 also had reduced proteins controlling mRNA surveillance and RNA processing. Transmission electron microscopy of hyphal cross sections confirmed that T625 formed abnormally enlarged endosomes or vacuoles. These data reveal that Blistering1 affects internal and external protein processing involving vesicle-mediated transport in a family of fungi with medical, commercial, and agricultural importance.

Original languageEnglish (US)
Pages (from-to)344-361
Number of pages18
JournalMolecular and Cellular Proteomics
Volume19
Issue number2
DOIs
StatePublished - Jan 1 2020

All Science Journal Classification (ASJC) codes

  • Analytical Chemistry
  • Biochemistry
  • Molecular Biology

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    Jurick, W. M., Peng, H., Beard, H. S., Garrett, W. M., Lichtner, F. J., Luciano-Rosario, D., Macarisin, O., Liu, Y., Peter, K. A., Gaskins, V. L., Yang, T., Mowery, J., Bauchan, G., Keller, N. P., & Cooper, B. (2020). Blistering1 modulates penicillium expansum virulence via vesicle-mediated protein secretion. Molecular and Cellular Proteomics, 19(2), 344-361. https://doi.org/10.1074/mcp.RA119.001831