Mechanisms and significance of fungicide resistance

Abstract

In this review article, we show that occurrence of fungicide resistance is one of the most important issues in modern agriculture. Fungicide resistance may be due to mutations of genes encoding fungicide targets (qualitative fungicide resistance) or to different mechanisms that are induced by sub-lethal fungicide stress. These mechanisms result in different and varying levels of resistance (quantitative fungicide resistance). We discuss whether or not extensive use of fungicides in agricultural environments is related to the occurrence of fungicide resistance in clinical environments. Furthermore, we provide recommendations of how development of fungicide resistant pathogen populations may be prevented or delayed.

Keywords: Citrus black spot disease; disease management; efflux transporters; fungicide resistance; wheat tan spot disease.

Figure 1:

Efficacy of sterol biosynthesis inhibitor fungicides in in vitro and in vivo against the causal agent of citrus black spot disease, Guignardia citricarpa. Growth on control PDA plates without fungicide (Fig. 1a) and on plates containing 200 ppm imazalil (Fig. 1b) indicated that G. citricarpa can not be completely controlled, even at high concentrations of this fungicide. Accordingly, infection assays on non-treated orange fruits (Citrus sinensis var. Valência) (Fig. 1c) and fruits treated with thiabendazole at recommended concentrations (5 ppm) (Fig. 1d) indicated failure of fungicide treatment. Data from Toffano (54).

Figure 2:

Development of fungicide resistance is a selection process, with the fungicide as the selecting agent. In qualitative resistance (Fig. 2a), mutation-based insensitive mutants are selected, and strains are either sensitive or resistant to the drug. In quantitative resistance (Fig. 2b) individuals that express genes leading to reduced fungicide sensitivity, are more likely to survive a drug treatment. Sub-lethal fungicide stress leads to further induction of genes that help resisting subsequent drug treatments. As a consequence the population is shifted to increasing resistance, and increasing numbers of individuals with higher degrees of resistance are found. For details, see text. After Hewitt (22), modified.

Figure 3:

Diagram of a fungal ABC- and an MFS-transporter. The ABC transporter consists of two repeats of a nucleotide binding domain (NBF) and six trans-membrane domains; the MSF transporter has 12 trans-membrane domains. The membrane efflux pumps can transport structurally diverse molecules such as strobilurin and azole fungicides, the fluorescent dye ethidium bromide, and the plant defense compounds resveratrol and resorcinol. After Del Sorbo et al. (13), modified.

Figure 4:

Adaptation of Pyrenophora tritici-repentis to fungicides. Different isolates (Fig. 4A; I, II and III) were allowed to adapt to different concentrations (Fig. 4A; 1, 5 and 10 ppm) of a strobilurin fungicide and plated out on agar plates containing 50 ppm of the same fungicide. Non-adapted control isolates (Fig. 4A; 0) were unable to grow. Isolates adapted to three different strobilurin fungicides (Fig. 4B; positions b, c and d) and an isolate adapted to an azole fungicide (Fig. 4B; position e) were able to grow on a plate containing 50 ppm of a strobilurin fungicide. A non-adapted control isolate (Fig. 4B; position a) did not grow.