Soil cadmium stress affects phyllosphere microbiome and associated pathogen resistance differently in male and female poplars.

Phyllosphere associated microorganisms play a crucial role in protecting plants from diseases, while their composition and diversity are strongly influenced by heavy metal contaminants. As dioecious plants exhibited sexual dimorphism in metal accumulation and tolerance between male and female individuals, in this study we used male and female full-sibs of Populus deltoides to investigate whether the two plant sexes will present sexual differences in the phyllosphere microbiome structure and associated pathogen resistance against a leaf pathogenic fungus after soil cadmium (Cd) exposure. We found that Cd-treated male plants grew better and accumulated more leaf Cd than females. Cd stress reduced leaf lesion area of both plant sexes after leaf pathogen infection, whereas male plants exhibited better resistance than females. More importantly, Cd exposure differentially altered the structure and function of phyllosphere microbiomes between male and female plants, with more abundant ecologically beneficial microbes but decreased pathogenic fungal taxa harbored in male plants. Further in vitro toxicity tests suggested that such sexual difference in pathogen resistance between the two plant sexes could attribute to direct Cd toxicity and indirect shifts in the phyllosphere microbiome. This study provides implication for understanding the underlying mechanism of heavy metals involved in plant-pathogen interactions.