Competitive exclusion amongst endophytes determines shoot blight severity on pine

Abstract

The role of competitive interactions among endophytes and latent pathogens that determine disease on stressed plants is largely unknown. Shoot blight caused by Diplodia sapinea is an emerging disease affecting pine forests in Europe. D. sapinea is an endophyte that becomes pathogenic following drought or hail. Disease expression depends on the availability of nutrient-rich metabolites produced by trees to alleviate stress. We studied whether competition for these compounds with other endophytes could modulate symptom expression. We compared the shoot-inhabiting fungal community of trees that developed blight symptoms or remained asymptomatic following a hailstorm that affected four pine species. Communities were characterised by isolation and metabarcoding of the ITS2 region. Endophytes were functionally annotated in their response to C, N and proline. Hail promoted D. sapinea and other endophytes with a rapid colonisation strategy of N-rich substrates. Asymptomatic trees had a community of endophytes showing a strong negative association with D. sapinea. These antagonistic endophytes were functionally similar to D. sapinea in their response traits to hail, but they were more specialised to proline. The association was conserved across pine species. Our data suggest that after a stress-inducing event, rapid niche occupation is critical for D. sapinea to cause disease. However, competition with other endophytes for key metabolites can supress the pathogen and prevent trees from developing symptoms. Our findings can pave the way to a better understanding of the contribution of latent pathogens on widespread tree mortality events involving abiotic stressors, such as drought, heat or hail. A free Plain Language Summary can be found within the Supporting Information of this article.