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Eukaryotic Cell, August 2006, p. 1399-1409, Vol. 5, No. 8
1535-9778/06/$08.00+0     doi:10.1128/EC.00131-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

The vtc4 Gene Influences Polyphosphate Storage, Morphogenesis, and Virulence in the Maize Pathogen Ustilago maydis

Kylie J. Boyce,{dagger} Matthias Kretschmer,{ddagger} and James W. Kronstad*

The Michael Smith Laboratories, Department of Microbiology and Immunology, and Faculty of Land and Food Systems, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4

Received 5 May 2006/ Accepted 9 June 2006

The maize pathogen Ustilago maydis switches from budding to filamentous, dikaryotic growth in response to environmental signals including nutrient status, growth in the host, and the presence of mating pheromones. The filamentous dikaryon is capable of proliferating within host tissue to cause disease symptoms including tumors. The transition from yeast cells to hyphal filaments is regulated by a mitogen-activated protein kinase cascade and a cyclic-AMP-protein kinase A (PKA) pathway. Serial analysis of gene expression with PKA mutants identified orthologs of components of the PHO phosphate acquisition pathway as transcriptional targets of the PKA pathway, and these included genes for Pho84, an acid phosphatase, and the vacuolar transport chaperones Vtc1 and Vtc4. In Saccharomyces cerevisiae, Vtc4p is required during the fusion of inorganic-phosphate-containing vesicles to the vacuolar membrane and the consequent accumulation of phosphate stored as polyphosphate (polyP) in the vacuole. We found that deletion of vtc4 in U. maydis also reduced polyP stored in vacuoles. Intriguingly, {Delta}vtc4 mutants possessed a filamentous cellular morphology, in contrast to the budding, yeast-like growth of the wild-type parent. The {Delta}vtc4 mutants also displayed decreased symptom development and reduced proliferation in planta. The interaction with PKA signaling was further investigated by the generation of {Delta}vtc4 ubc1 double mutants. Deletion of vtc4 completely suppressed the multiple-budded phenotype of a {Delta}ubc1 mutant, indicating that polyP stores are essential for this PKA-induced trait. Overall, this study reveals a novel role for PKA-regulated polyP accumulation in the control of fungal morphogenesis and virulence.

* Corresponding author. Mailing address: The Michael Smith Laboratories, Department of Microbiology and Immunology, and Faculty of Land and Food Systems, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4. Phone: (604) 822-4732. Fax: (604) 822-2114. E-mail: Kronstad{at}interchange.ubc.ca.

{dagger} Present address: Department of Genetics, University of Melbourne, Melbourne, Victoria, Australia 3010.

{ddagger} Present address: University of Kaiserslautern, Department of Biology, Phytopathology Group, 67663 Kaiserslautern, Germany.

Eukaryotic Cell, August 2006, p. 1399-1409, Vol. 5, No. 8
1535-9778/06/$08.00+0     doi:10.1128/EC.00131-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.





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