An ABC Transporter and a Cytochrome P450 of Nectria haematococca MPVI Are Virulence Factors on Pea and Are the Major Tolerance Mechanisms to the Phytoalexin Pisatin

Abstract

The fungal plant pathogen Nectria haematococca MPVI produces a cytochrome P450 that is responsible for detoxifying the phytoalexin pisatin, produced as a defense mechanism by its host, garden pea. In this study, we demonstrate that this fungus also produces a specific ATP-binding cassette (ABC) transporter, NhABC1, that enhances its tolerance to pisatin. In addition, although both mechanisms individually contribute to the tolerance of pisatin and act as host-specific virulence factors, mutations in both genes render the fungus even more sensitive to pisatin and essentially nonpathogenic on pea. NhABC1 is rapidly induced after treatment with pisatin in vitro and during infection of pea plants. Furthermore, NhABC1 was able to confer tolerance to the phytoalexin rishitin, produced by potato. NhABC1 appears to be orthologous to GpABC1 of the potato pathogen Gibberella pulicaris and, along with MoABC1 from Magnaporthe oryzae, resides in a phylogenetically related clade enriched with ABC transorters involved in virulence. We propose that NhABC1 and the cytochrome P450 may function in a sequential manner in which the energy expense from pisatin efflux by NhABC1 releases the repression of the cytochrome P450, ultimately allowing pisatin tolerance by two mechanisms. These results demonstrate that a successful pathogen has evolved multiple mechanisms to overcome these plant antimicrobial compounds.

Gene Discovery for Enzymes Involved in Limonene Modification or Utilization by the Mountain Pine Beetle-Associated Pathogen Grosmannia clavigera

“…While most of the MPB-associated fungi can use monoterpenes (i.e., limonene) as a carbon source, one of the Grosmannia cryptic species (Gc from Jeffrey pine) and the saprophyte were unable to. Successful plant and animal pathogens, such as Nectria haematococca and other fungi, use multiple mechanisms for detoxifying plant antimicrobial compounds (41), and our results indicate that this is also the case for Gs. In previous work, we showed that a fungal ABC efflux transporter was a major mechanism by which Gs copes with the diffusion of monoterpenes into its cells in artificial media or when inoculated into young pine trees.…”

Expression Profiling of the Wheat Pathogen Zymoseptoria tritici Reveals Genomic Patterns of Transcription and Host-Specific Regulatory Programs

“…Determinants of host specificity and virulence have been identified on ACs of other fungal plant pathogens, including the AC-encoded enzymes for detoxification of a plant phytoalexin in Nectria haematococca (Miao et al . 1991; Coleman et al . 2011) and the virulence-associated host-specific effector genes on lineage-specific chromosomes of Fusarium oxysporum (Ma et al .…”

The Full-Size ABCG Transporters Nb-ABCG1 and Nb-ABCG2 Function in Pre- and Postinvasion Defense against Phytophthora infestans in Nicotiana benthamiana

“…Interestingly, there are several examples showing that ABC transporters of plant pathogenic fungi are likewise responsible for the efflux of plant-derived defense compounds. These include atrB of B. cinerea, which transports grapevine (Vitis vinifera) resveratrol, ABC1 of Nectria hematococca, which transports pea (Pisum sativum) pisatin, and ABC-G1 of Grosmannia clavigera, which transports pine (Pinus contorta) monoterpenes (Schoonbeek et al, 2001;Coleman et al, 2011;Wang et al, 2013).…”