Seed microbiomes promote Astragalus mongholicus seed germination through pathogen suppression and cellulose degradation

BACKGROUND: Seed-associated microorganisms play crucial roles in maintaining plant health by providing nutrients and resistance to biotic and abiotic stresses. However, their functions in seed germination and disease resistance remain poorly understood. In this study, we investigated the microbial community assembly features and functional profiles of the spermosphere and endosphere microbiomes related to germinated and ungerminated seeds of Astragalus mongholicus by using amplicon and shotgun metagenome sequencing techniques. Additionally, we aimed to elucidate the relationship between beneficial microorganisms and seed germination through both in vitro and in vivo pot experiments. RESULTS: Our findings revealed that germination significantly enhances the diversity of microbial communities associated with seeds. This increase in diversity is driven through environmental ecological niche differentiation, leading to the enrichment of potentially beneficial probiotic bacteria such as Pseudomonas and Pantoea. Conversely, Fusarium was consistently enriched in ungerminated seeds. The co-occurrence network patterns revealed that the microbial communities within germinated and ungerminated seeds presented distinct structures. Notably, germinated seeds exhibit more complex and interconnected networks, particularly for bacterial communities and their interactions with fungi. Metagenome analysis showed that germinated seed spermosphere soil had more functions related to pathogen inhibition and cellulose degradation. Through a combination of culture-dependent and germination experiments, we identified Fusarium solani as the pathogen. Consistent with the metagenome analysis, germination experiments further demonstrated that bacteria associated with pathogen inhibition and cellulose degradation could promote seed germination and vigor. Specifically, Paenibacillus sp. significantly enhanced A. mongholicus seed germination and plant growth. CONCLUSIONS: Our study revealed the dynamics of seed-associated microorganisms during seed germination and confirmed their ecological role in promoting A. mongholicus seed germination by suppressing pathogens and degrading cellulose. This study offers a mechanistic understanding of how seed microorganisms facilitate successful seed germination, highlighting the potential for leveraging these microbial communities to increase plant health. Video Abstract.