Research advances on plant phyllosphere microorganisms and their responses to fertilization

Phyllosphere microorganisms, constituting a distinct microbial assemblage colonizing the aerial surfaces of plants, perform pivotal ecological functions within plant-associated ecosystems. Advances in high-throughput sequencing and metagenomic technologies have revolutionized research into this unique microbial habitat. Using the “China National Knowledge Infrastructure (CNKI)” and “Web of Science”core databases, we searched literature published from January 2000 to June 2023, using “phyllosphere microorganism”as a keyword. A total of 93 relevant Chinese articles and 498 foreign articles were retrieved. The key findings by bibliometric analysis revealed that research on plant disease control and biological control, characterized by high co-occurrence intensity and sustained research interest, has become one of the core research directions in this field. In addition, the relationships among soil microorganisms, rhizosphere microorganisms, and phyllosphere microorganisms are also a current research focus. Emerging evidences highlighted the multifaceted roles of phyllosphere communities: enhancing host stress tolerance, contributing to nitrogen fixation, and impacting human health through microbial dissemination. Their colonization process is governed by complex interactions between host-specific traits (e.g., leaf structure and phytochemical profiles) and environmental variables (e.g., climatic regimes and edaphic conditions). In intensive agricultural production, fertilization practices represent crucial management levers that significantly reshape crop physiology and microenvironmental conditions, thereby exerting profound influences on phyllosphere community assembly. This review synthesizes current understanding of how fertilizer types, application dosages, and delivery methods modulate the structural and functional attributes of crop phyllosphere microbiota. Novel strategies are proposed for manipulating leaf traits via optimized fertilization regimes to engineer beneficial microbial consortia, while maintaining phyllosphere homeostasis for sustainable plant health. To advance the field, four priority research avenues are identified: 1) Mechanistic insights: Deciphering mineral nutrient-mediated regulation of phyllosphere microbial interactions; 2) Microbial transmission networks: Characterizing fertilizer-driven dispersal patterns across the soil-plant continuum; 3) Biosafety evaluations: Assessing risks associated with organic fertilizer-induced phyllosphere microbial introductions; 4) Agrobiotechnology innovation: Exploring phyllosphere microbial resources to enhance nutrient use efficiency and agricultural products quality. These investigative trajectories promise to deepen our ecological comprehension of phyllosphere microbiota while unlocking their biotechnological potential for sustainable agriculture. By integrating multi-omics approaches with field-scale validations, future studies can establish foundational principles for harnessing phyllosphere microbial diversity to address global food security challenges.