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Edited* by Jay C. Dunlap, Dartmouth Medical School, Hanover, NH, and approved January 11, 2011 (received for review November 23, 2010)
Abstract
Regulated synthesis of reactive oxygen species (ROS) by membrane-bound fungal NADPH oxidases (Nox) plays a key role in fungal morphogenesis, growth, and development. Generation of reactive oxygen species (ROS) by the plant symbiotic fungus, Epichloë festucae, requires functional assembly of a multisubunit complex composed of NoxA, a regulatory component, NoxR, and the small GTPase RacA. However, the mechanism for assembly and activation of this complex at the plasma membrane is unknown. We found by yeast two-hybrid and coimmunoprecipitation assays that E. festucae NoxR interacts with homologs of the yeast polarity proteins, Bem1 and Cdc24, and that the Phox and Bem1 (PB1) protein domains found in these proteins are essential for these interactions. GFP fusions of BemA, Cdc24, and NoxR preferentially localized to actively growing hyphal tips and to septa. These proteins interact with each other in vivo at these same cellular sites as shown by bimolecular fluorescent complementation assays. The PB1 domain of NoxR is essential for localization to the hyphal tip. An E. festucae ΔbemA mutant was defective in hyphal morphogenesis and growth in culture and in planta. The changes in fungal growth in planta resulted in a defective symbiotic interaction phenotype. Our inability to isolate a Δcdc24 mutant suggests this gene is essential. These results demonstrate that BemA and Cdc24 play a critical role in localizing NoxR protein to sites of fungal hyphal morphogenesis and growth. Our findings identify a potential shared ancestral link between the protein machinery required for fungal polarity establishment and the Nox complex controlling cellular differentiation.
Footnotes
- 2To whom correspondence should be addressed. E-mail: d.b.scott{at}massey.ac.nz.
Author contributions: D.T. and B.S. designed research; D.T., S.K., S.S., Y.B., R.W., and A.T. performed research; D.T., S.S., Y.B., H.S., and B.S. analyzed data; and D.T. and B.S. wrote the paper.
↵1Present address: Michael Smith Laboratories, University of British Columbia, Vancouver, BC, Canada V6T1Z4.
The authors declare no conflict of interest.
Data deposition: The sequences reported in this paper have been deposited in the DDBJ/EMBL/GenBank databases (accession nos. AB524338 and AB524339).
↵*This Direct Submission article had a prearranged editor.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1017309108/-/DCSupplemental.
Freely available online through the PNAS open access option.
Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex
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