Cheating (re)shapes pathogen virulence and antifungal resistance
HM, S.; Pieterse, F. P. J.; van de Sande, M. A. J.; Bastiaans, E.; Debets, A. J.; Fleissner, A.; van Kan, J. A. L.
Show abstract
Filamentous fungi grow as fused, multinucleate networks that share secreted public goods vs private goods. We asked whether this sharing enables "cheater" nuclei to increase in frequency by exploiting goods produced by other nuclei, and whether such social conflict shapes virulence and antifungal resistance. We tested this in the gray mold pathogen Botrytis cinerea by contrasting an extracellular detoxification trait, a public good (enzymatic hydrolysis of the tomato saponin alpha-tomatine) with an intracellular antibiotic resistance trait, a private good (hygromycin phosphotransferase). In pairwise competitions, tomatinase-deficient nuclei gained advantage when rare against a constitutive producer, both in vitro and in planta, even though producers drive lesion expansion. An ordinary differential equation model fitted to the competition outcomes identified antibiotic gradients as the key driver of frequency-dependent selection and predicted stable coexistence of producer and non-producer nuclei across multinucleate bottlenecks. Cheating within fungal syncytia can therefore decouple virulence from reproduction and buffer the selection on antifungal resistance.
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