National-scale investigation reveals the dominant role of phyllosphere fungal pathogens in sorghum yield loss.

[Display omitted] • The diversity of fungal plant pathogens in the phyllosphere was higher than that in the rhizosphere. • Fungal pathogen diversity was significantly and negatively correlated with latitude in both phyllosphere and rhizosphere. • Climatic factors and soil properties were the most important factors influencing fungal pathogen diversity in phyllosphere and rhizosphere, respectively. • The phyllosphere fungal plant pathogen diversity plays a crucial role in sorghum yield. Fungal plant pathogens threaten crop production and sustainable agricultural development. However, the environmental factors driving their diversity and nationwide biogeographic model remain elusive, impacting our capacity to predict their changes under future climate scenarios. Here, we analyzed potential fungal plant pathogens from 563 samples collected from 57 agricultural fields across China. Over 28.0% of fungal taxa in the phyllosphere were identified as potential plant pathogens, compared to 22.3% in the rhizosphere. Dominant fungal plant pathogen groups were Cladosporium (in the phyllosphere) and Fusarium (in the rhizosphere), with higher diversity observed in the phyllosphere than in rhizosphere soil. Deterministic processes played an important role in shaping the potential fungal plant pathogen community assembly in both habitats. Mean annual precipitation and temperature were the most important factor influencing phyllosphere fungal plant pathogen richness. Significantly negative relationships were found between fungal pathogen diversity and sorghum yield. Notably, compared to the rhizosphere, the phyllosphere fungal plant pathogen diversity played a more crucial role in sorghum yield. Together, our work provides novel insights into the factors governing the spatial patterns of fungal plant pathogens in the crop microbiome, and highlights the potential significance of aboveground phyllosphere fungal plant pathogens in crop productivity. [ABSTRACT FROM AUTHOR]