Plant sex affects plant-microbiome assemblies of dioecious Populus cathayana trees under different soil nitrogen conditions

Abstract Background Dioecious plants have coevolved with diverse plant microbiomes, which are crucial for the fitness and productivity of their host. Sexual dimorphism in morphology, physiology, or gene expression may relate to different microbial compositions that affect male and female fitness in different environments. However, sex-specific impacts on ecological processes that control the microbiome assembly are not well known. In this study, Populus cathayana males and females were planted in different nitrogen conditions. It was hypothesized that males and females differently affect bacterial and fungal communities in the rhizosphere soil, roots, old leaves, and young leaves. Physiological traits and transcriptome profiles of male and female plants were investigated to reveal potential mechanisms that control the microbiome assembly. Results Our results showed strong niche differentiation that shapes microbial communities leading to a rapid loss of diversity along a decreasing pH gradient from the rhizosphere soil to leaves. Sex had different impacts on the microbial assembly in each niche. Especially fungal endophytes showed great differences in the community structure, keystone species, and community complexity between P. cathayana males and females. For example, the fungal co-occurrence network was more complex and the alpha diversity was significantly higher in young female leaves compared to young male leaves. Transcriptome profiles revealed substantial differences in plant-pathogen interactions and physiological traits that clearly demonstrated divergent internal environments for endophytes inhabiting males and females. Starch and pH of young leaves significantly affected the abundance of Proteobacteria, while tannin and pH of roots showed significant effects on the abundance of Chloroflexi, Actinobacteria, and Proteobacteria, and on the bacterial Shannon diversity. Conclusion Our results provided important knowledge for understanding sexual dimorphism that affects microbial assemblies, thus advancing our understanding of plant-microbiome interactions. Video Abstract