The Biotrophic, Non-Appressorium-Forming Grass Pathogen Claviceps purpurea Needs a Fus3/Pmk1 Homologous Mitogen-Activated Protein Kinase for Colonization of Rye Ovarian Tissue

Abstract

Claviceps purpurea is a common pathogen of a wide range of grasses and cereals that is able to establish a stable, balanced interaction with its host plant and is considered a biotroph. It does not form special penetration structures such as appressoria. To study the signaling processes involved in this special host-pathogen interaction, we have cloned a gene, cpmk1, encoding a mitogen-activated protein (MAP) kinase that shows significant homology to Fus3 of Saccharomyces cerevisiae and to pmk1 of Magnaporthe grisea. Using a gene-replacement approach, we isolated a Acpmk1 mutant and characterized it in detail. Loss of CPMK1 has no obvious effect on vegetative properties (such as growth rate, morphology, and conidia formation); however, infection tests on rye show that the mutant is unable to colonize rye tissue, i.e., it appears to be completely nonpathogenic. Complementation of the mutant with a wild-type copy of cpmk1 fully restores its pathogenicity, confirming that this MAP kinase is essential for infection of rye by C. purpurea. Transformation of the delta pmk1 mutant of M. grisea with a complete copy of cpmk1 (including the C. purpurea promoter) fully restored its ability to form appressoria and its pathogenicity on barley. Although both fungi drastically differ in their pathogenic strategies, this result indicates that the signal pathway involving CPMK1 is highly conserved.

Two Novel Fungal Virulence Genes Specifically Expressed in Appressoria of the Rice Blast Fungus

“…GMK1 from Gaeumannomyces graminis fully complemented the defects of the Magnaporthe pmk1 mutant in appressorial development and invasive growth, indicating that the function of PMK1 MAP kinase may be conserved in this root pathogen (Dufresne and Osbourn, 2001). Even in the biotrophic, nonappressorium-forming pathogen Claviceps purpurea , the PMK1 homolog is essential for colonizing rye ovarian tissues (Mey et al, 2002). These data suggest that the PMK1 pathway is conserved in many, if not all, fungi for appressorium formation and other plant infection processes.…”

Mitogen-Activated Protein Kinase Signaling in Plant-Interacting Fungi: Distinct Messages from Conserved Messengers

“…The function of Kss1/Fus3-type MAPKs was also assessed in biotrophic fungi, including the hemibiotroph pathogen Claviceps purpurea (Mey et al, 2002b). C. purpurea mutants lacking the MAPK gene mk1 (here renamed Cpu-Kss1) are nonpathogenic, while complementation assays reveal that Cpu-Kss1 can rescue M. oryzae strains lacking their corresponding Kss1 gene.…”

A Mitogen-Activated Protein Kinase Cascade Regulating Infection-Related Morphogenesis in Magnaporthe grisea

“…Similar to pmk1 mutants in M. grisea, gene replacement mutants of PTK1 in P. teres and CMK1 in C. lagenarium are nonpathogenic and fail to colonize healthy or wounded host tissues (Takano et al, 2000;Ruiz-Roldan et al, 2001). PMK1 homologs are also important for fungal pathogenicity in several filamentous ascomycetes, including Botrytis cinerea, Gibberella zeae, Fusarium oxysporum f sp lycopersici, and Claviceps purpurea (Di Pietro et al, 2001;Mey et al, 2002;Jenczmionka et al, 2003). In the basidiomycete Ustilago maydis, two MAPKs, ubc3 (kpp2) and kpp6, are similar to other fungal MAPKs involved in mating and pathogenicity (Kahmann and Kamper, 2004).…”