Special Interest Group Meeting

Tête à tête inside a plant cell: the intracellular infection structures of biotrophic fungal pathogens

Richard O’Connell, Hiroyuki Takahara and Jochen Kleemann, Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, Cologne 50829, Germany

The interaction between the model plant Arabidopsis thaliana and the hemibiotrophic ascomycete Colletotrichum higginsianum provides a model pathosystem in which both pathogen and host can be genetically manipulated and genome sequences are available for both partners. The fungal infection process involves sequential differentiation of a series of specialised cell-types (infection structures). After initial host penetration by melanized appressoria, the fungus grows biotrophically inside living epidermal cells, producing bulbous biotrophic hyphae that invaginate and expand the host plasma membrane and remodel the host cytoplasm. To obtain insights into the functions of these biotrophic hyphae, we used 454-pyrosequencing to survey the transcriptome of hyphae purified from infected leaves by fluorescence-activated cell sorting. We found homologs of many genes related to redox homeostasis, biosynthesis of proteins, amino acids and vitamins, and uptake of amino acids, mono- and disaccharides. Using computational prediction tools, we identified fungal genes encoding small, soluble secreted proteins which may function as effectors for host manipulation. Expression profiling showed many candidate effector genes to be plant-induced and highly stage-specific. Localization in planta, by immunolabelling or ectopic expression of fluorescent fusion proteins in C. higginsianum, revealed that several effectors accumulate at the plant-fungal interface. We present evidence that some effectors function in counter-defense, potentially masking fungal cell wall components from detection by plant PAMP receptors, while others may suppress plant cell death. Overall, our findings suggest that, similar to the haustoria of obligate parasites, Colletotrichum biotrophic hyphae function in nutrient uptake and delivery of effector proteins into host cells.