Fungicide-free management of Alternaria leaf blotch and fruit spot on apple indicates Alternaria spp. as secondary colonizer

The fungal genus Alternaria is a pan-global pathogen of > 100 crops, and is associated with the globally expanding Alternaria leaf blotch in apple (Malus x domestica Borkh.) which leads to severe leaf necrosis, premature defoliation, and large economic losses. Up to date, the epidemiology of many Alternaria species is still not resolved as they can be saprophytic, parasitic or shift between both lifestyles and are also classified as primary pathogen able to infect healthy tissue. We argue that Alternaria spp. does not act as primary pathogen, but only as a necrosis-dependent opportunist. We studied the infection biology of Alternaria spp. under controlled conditions and monitored disease prevalence in real orchards and validated our ideas by applying fungicide-free treatments in 3-years field experiments. Alternaria spp. isolates were not able to induce necroses in healthy tissue, but only when prior induced damages existed. Next, leaf-applied fertilizers, without fungicidal effect, reduced Alternaria-associated symptoms (- 72.7%, SE: ± 2.5%) with the same efficacy as fungicides. Finally, low leaf magnesium, sulphur, and manganese concentrations were consistently linked with Alternaria-associated leaf blotch. Fruit spot incidence correlated positively with leaf blotch, was also reduced by fertilizer treatments, and did not expand during storage unlike other fungus-mediated diseases. Our findings suggest that Alternaria spp. may be a consequence of leaf blotch rather than its primary cause, as it appears to colonize the physiologically induced leaf blotch. Taking into account existing observations that Alternaria infection is connected to weakened hosts, the distinction may appear slight, but is of great significance, as we can now (a) explain the mechanism of how different stresses result in colonization with Alternaria spp. and (b) substitute fungicides for a basic leaf fertilizer. Therefore, our findings can result in significant decreases in environmental costs due to reduced fungicide use, especially if the same mechanism applies to other crops.