title: Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato.
abstract: Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during the colonization of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but are repressed during the biotrophic phase of tomato colonization. It has been suggested that the tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, whilst retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato in a similar manner to the wild-type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which, in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low-temperature stress. Overall, this study demonstrates that the repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, whereas its production is important for survival outside its host.
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.
authors.forename: Scott
authors.initials: S
authors.lastname: Griffiths
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.
authors.forename: Carl H
authors.initials: CH
authors.lastname: Mesarich
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.|Laboratory of Cell Biology, Wageningen University, Wageningen, 6708 PB, the Netherlands.
authors.forename: Elysa J R
authors.initials: EJR
authors.lastname: Overdijk
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.
authors.forename: Benedetta
authors.initials: B
authors.lastname: Saccomanno
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.
authors.forename: Pierre J G M
authors.initials: PJGM
authors.lastname: de Wit
authors.affiliation: Laboratory of Phytopathology, Wageningen University, Wageningen, 6708 PB, the Netherlands.|UMR1345 Institut de Recherche en Horticulture et Semences (IRHS)-INRA, ACO, Université d'Angers, Beaucouzé Cedex, 49071, France.
authors.forename: Jérôme
authors.initials: J
authors.lastname: Collemare
mesh_terms: D001688:Biological Products / Q000378:metabolism; D002963:Cladosporium / Q000378:metabolism* / Q000472:pathogenicity*; D005656:Fungal Proteins / Q000235:genetics / Q000378:metabolism*; D015966:Gene Expression Regulation, Fungal; D010935:Plant Diseases / Q000382:microbiology*; D014774:Virulence
chemical_list: D001688:Biological Products; D005656:Fungal Proteins
keywords: Fulvia fulva; abiotic stress resistance; biotrophy; natural product; regulation of secondary metabolism; virulence