Host phylogeny and traits shape the composition and network structure of the phyllosphere microbial communities in temperate desert plants

Abstract

Phyllosphere microorganisms play a vital role in enhancing the adaptability and functionality of their host plants. Although the effects of phyllosphere microbial communities on host functional traits and their association with host phylogeny has been widely investigated, it remains unclear whether host selection consistently drives the assembly of these communities. In this study, bacterial and fungal communities on the surfaces of 734 leaf samples were characterized using bacterial and fungal amplicon sequencing. These microbial communities were associated with 42 plant species native to the Gurbantunggut Desert, a representative temperate desert located in Central Asia. The research assessed the relative contributions of plant-related factors, abiotic environmental variables (such as climate and soil), and spatial components to the observed variation in phyllosphere microbial communities, and further inferred the topological structure of plant-microbe interaction networks. The results indicate that plant phylogeny, plant functional traits, abiotic environment conditions, and spatial factors account for variations in the bacterial community composition (36.4 %, 4.6 %, 1.0 %, and 0.1 %, respectively) and the fungal community composition (28.6 %, 3.0 %, 1.5 %, and 1.2 %, respectively), following a hierarchical trend of plant phylogeny > plant functional traits > abiotic environment > space. Plant phylogeny and functional traits play a central role in shaping the assembly of phyllosphere microbial communities, indicating that plant filtering effects significantly influence microbial composition. Analysis of plant-microbe interactions reveals distinct preferences of microbial taxa for plant hosts across different taxonomic levels and geographic regions. Bipartite network analysis further illustrates that plant-microbe networks are highly specialized and modular, with plant-fungal networks exhibiting greater host specificity compared to plant-bacterial networks. Collectively, these findings underscore plant filtering as the primary determinant of microbial community assembly in the desert phyllosphere and provide valuable insights into the macroecological patterns shaping plant-microbe interactions in arid ecosystems.