Narrow, but not broad, spectrum resistance and disease reshape phyllosphere bacterial communities

Abstract

The phyllosphere is a restrictive environment for microbes, resulting in microbial communities typically dominated by select taxa with specific adaptations for success in this niche. However, biotic stress, especially from plant disease, could disrupt this environment in ways that alter the resulting phyllosphere community, with potential consequences for plant and human health. Additionally, plant disease resistance, through both broad (pattern-triggered immunity) and specific (effector-triggered immunity) resistance, could affect non-pathogenic communities directly or indirectly via effects on disease progression. Here, we tested how transgenic ETI and PTI resistance genes affected the phyllosphere communities of tomato plants in the face of infection by Xanthomonas perforans and the resulting bacterial spot disease. We found that the expression of the Bs2 transgene (ETI) had major effects on phyllosphere communities, while the EFR (PTI) transgene did not. The effect of the Bs2 resistance gene could be largely attributed to the change in disease symptoms. Diseased leaves harbored reduced bacterial diversity and reductions in major phyllosphere inhabitants (e.g. Sphinogmonas and Methylobacterium), while a limited number of bacterial genera showed increased relative abundance on diseased leaves. These results suggest that phyllosphere communities are sensitive to the direct and indirect effects of plant disease and resistance, and the consequences of these shifts for plant and human health deserve further investigation.