Elevated CO2 reduces disease incidence and severity of a red maple fungal pathogen via changes in host physiology and leaf chemistry

Atmospheric CO₂ concentrations are predicted to double within the next century. Despite this trend, the extent and mechanisms through which elevated CO₂ affects plant diseases remain uncertain. In this study, we assessed how elevated CO₂ affects a foliar fungal pathogen, Phyllosticta minima, of Acer rubrum growing in the understory at the Duke Forest free‐air CO₂ enrichment experiment in Durham, North Carolina. Surveys of A. rubrum saplings in the 6th, 7th, and 8th years of the CO₂ exposure revealed that elevated CO₂ significantly reduced disease incidence, with 22%, 27%, and 8% fewer saplings and 14%, 4%, and 5% fewer leaves infected per plant in the three consecutive years, respectively. Elevated CO₂ also significantly reduced disease severity in infected plants in all years (e.g. mean lesion area reduced 35%, 50%, and 10% in 2002, 2003, and 2004, respectively). To assess the mechanisms underlying these changes, we combined leaf structural, physiological and chemical analyses with growth chamber studies of P. minima growth and host infection. In vitro exponential growth rates of P. minima were enhanced by 17% under elevated CO₂, discounting the possibility that disease reductions were because of direct negative effects of elevated CO₂ on fungal performance. Scanning electron micrographs (SEM) verified that conidia germ tubes of P. minima infect A. rubrum leaves by entering through the stomata. While stomatal size and density were unchanged, stomatal conductance was reduced by 21–36% under elevated CO₂, providing smaller openings for infecting germ tubes. Reduced disease severity under elevated CO₂ was likely due to altered leaf chemistry and reduced nutritive quality; elevated CO₂ reduced leaf N by 20% and increased the C : N ratio by 20%, total phenolics by 15%, and tannins by 14% (P<0.05 for each factor). The potential dual mechanism we describe here of reduced stomatal opening and altered leaf chemistry that results in reduced disease incidence and severity under elevated CO₂ may be prevalent in many plant pathosystems where the pathogen targets the stomata.