Wide distribution of resistance to the fungicides fludioxonil and iprodione in Penicillium species

• Published in: PloS one 2022-01, Vol.17 (1), p.e0262521-e0262521
• Main Authors: Oiki, Sayoko, Yaguchi, Takashi, Urayama, Syun-Ichi, Hagiwara, Daisuke
• Format: Article
• Language: English
• Subjects: Agricultural land; Agricultural research; Aminoimidazole Carboxamide - analogs & derivatives; Aminoimidazole Carboxamide - pharmacology; Antifungal agents; Biology and Life Sciences; Cadaver; Crop residues; Crops, Agricultural - microbiology; Dioxoles - pharmacology; Distribution; Drug resistance; Drug resistance in microorganisms; Drug Resistance, Fungal; Environmental science; Fludioxonil; Food Analysis; Fungal Proteins - genetics; Fungi; Fungicides; Fungicides, Industrial - pharmacology; Genetic aspects; Genomes; Genomics; Glycerol; Histidine; Histidine kinase; Humans; Hydantoins - pharmacology; Iprodione; Kinases; Laboratories; Lead compounds; Medicine and Health Sciences; Mode of action; Multidrug resistance; Mutation; Mycoses - drug therapy; Mycoses - genetics; Mycoses - microbiology; Nucleotides; Osmolarity; Pathogens; Penicillium; Penicillium - drug effects; Penicillium - genetics; Penicillium - isolation & purification; Pesticides; Physiological aspects; Plant protection; Polymorphism, Single Nucleotide; Pyrroles - pharmacology; Single-nucleotide polymorphism; Species
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0262521

Fludioxonil and iprodione are effective fungicides widely used for crop protection and are essential for controlling plant pathogenic fungi. The emergence of fungicide-resistant strains of targeted pathogens is regularly monitored, and several cases have been reported. Non-targeted fungi may also be exposed to the fungicide residues in agricultural fields. However, there are no comprehensive reports on fungicide-resistant strains of non-targeted fungi. Here, we surveyed 99 strains, representing 12 Penicillium species, that were isolated from a variety of environments, including foods, dead bodies, and clinical samples. Among the Penicillium strains, including non-pathogenic P. chrysogenum and P. camembertii, as well as postharvest pathogens P. expansum and P. digitatum, 14 and 20 showed resistance to fludioxonil and iprodione, respectively, and 6 showed multi-drug resistance to the fungicides. Sequence analyses revealed that some strains of P. chrysogenum and Penicillium oxalicum had mutations in NikA, a group III histidine kinase of the high-osmolarity glycerol pathway, which is the mode of action for fludioxonil and iprodione. The single nucleotide polymorphisms of G693D and T1318P in P. chrysogenum and T960S in P. oxalicum were only present in the fludioxonil- or iprodione-resistant strains. These strains also exhibited resistance to pyrrolnitrin, which is the lead compound in fludioxonil and is naturally produced by some Pseudomonas species. This study demonstrated that non-targeted Penicillium strains distributed throughout the environment possess fungicide resistance.