Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals

• Published in: Nature (London) Vol. 527; no. 7579; pp. 521 - 524
• Main Authors: Turrà, David, El Ghalid, Mennat, Rossi, Federico, Di Pietro, Antonio
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 26.11.2015; Nature Publishing Group
• Subjects: 42/35; 42/41; 42/70; 631/326/193/2542; 631/326/193/2544; 631/449/2676/2677; 82/58; 96/63; Amino acids; Catalysis; Cell receptors; Flowers & plants; Fungi; Fungi, Pathogenic; Fusarium - growth & development; Fusarium - metabolism; Host-parasite relationships; Host-Pathogen Interactions; Humanities and Social Sciences; Hyphae - growth & development; Hyphae - metabolism; Kinases; letter; Lycopersicon esculentum - enzymology; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - microbiology; MAP Kinase Signaling System; Mating Factor; Microbiological research; Molecular weight; multidisciplinary; Nutrient sources; Pathogens; Peptides - metabolism; Peroxidases - metabolism; Pheromones; Physiological aspects; Plant biology; Plant Roots - enzymology; Plant Roots - microbiology; Proteins; Receptors, Mating Factor - chemistry; Receptors, Mating Factor - metabolism; Science; Signal transduction; Tomatoes; Tropism - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature15516

Fungal pathogens reorient hyphal growth towards their plant hosts in response to chemical signals; here, directed growth of the plant pathogen Fusarium oxysporum towards the roots of the tomato plant is shown to be triggered by class III peroxidases secreted by the tomato plant, with the fungal response requiring a sex pheromone receptor. Plant sex hormome attracts fungal pathogen Fungal pathogens reorient hyphal growth towards their plant hosts in response to chemical signals, but the mechanisms involved have been unknown. In this study, Antonio di Pietro and colleagues show that directed growth of the plant pathogen Fusarium oxysporum towards the roots of the tomato plant ( Solanum lycopersicum ) is triggered by class III peroxidases that are secreted by the plant, and the fungal response requires the transmembrane protein Ste2, a homologue of the yeast sex pheromone α receptor. They go on to show that signalling through MAPK cascades is responsible for directing the growth of F. oxysporum , with functionally distinct cascades responding to different chemical signals. These results suggest a possible role for the fungal pheromone-sensing machinery in locating plant hosts in a complex environment such as the soil. For more than a century, fungal pathogens and symbionts have been known to orient hyphal growth towards chemical stimuli from the host plant 1 , 2 . However, the nature of the plant signals as well as the mechanisms underlying the chemotropic response have remained elusive 3 . Here we show that directed growth of the soil-inhabiting plant pathogen Fusarium oxysporum towards the roots of the host tomato ( Solanum lycopersicum ) is triggered by the catalytic activity of secreted class III peroxidases, a family of haem-containing enzymes present in all land plants 4 . The chemotropic response requires conserved elements of the fungal cell integrity mitogen-activated protein kinase (MAPK) cascade 5 and the seven-pass transmembrane protein Ste2, a functional homologue of the Saccharomyces cerevisiae sex pheromone α receptor 6 . We further show that directed hyphal growth of F. oxysporum towards nutrient sources such as sugars and amino acids is governed by a functionally distinct MAPK cascade. These results reveal a potentially conserved chemotropic mechanism in root-colonizing fungi, and suggest a new function for the fungal pheromone-sensing machinery in locating plant hosts in a complex environment such as the soil.