Inoculation of <i>Bacillus velezensis</i> SD24 enhancing the accumulation of tea catechin secondary metabolites

ABSTRACT Tea ( Camellia sinensis ) is a globally significant economic crop, and its desirable quality and health benefits are largely credited to catechin derivatives. Plant growth-promoting rhizobacteria (PGPR), such as Bacillus velezensis , are well-known for enhancing the environmental fitness and disease resistance of plants. However, the regulation of their impact on tea catechin biosynthesis remains unclear. While previous studies have focused on PGPR-facilitated growth promotion in crops like tomatoes and rice, the physiological mechanisms by which microbes regulate secondary metabolism in tea—especially under co-inoculation conditions—remain largely underexplored. This study examined the effects of B. velezensis SD24, isolated from tea rhizosphere soil, on catechin derivative accumulation of tea leaves by altering gene expression and the rhizosphere microbiome. Strain SD24 exhibited broad-spectrum antimicrobial activity against various pathogens due to behaving antimicrobial gene clusters. Tea plants inoculated with SD24 showed significantly increased levels of catechin derivatives in their leaves. This was likely achieved by upregulation of leucoanthocyanidin reductase and anthocyanidin reductase within the phenylpropanoid pathway. Additionally, chlorophyll content was increased. Transcriptomic analysis revealed a notable enrichment in biosynthesis of secondary natural products among the tea genes activated by SD24 inoculation. Metagenomic analysis further demonstrated that SD24 inoculation led to a restructuring of the tea rhizosphere microbiome. Notably, co-inoculation with Piriformospora indica , a beneficial endophytic fungus, suppressed SD24-induced gene expression and catechin accumulation, underscoring its antagonism toward SD24. These findings suggest that B. velezensis SD24 enhances tea quality, probably by transcriptionally activating the synthesis of catechin derivatives, a process associated with the restructuring of the rhizosphere microbiome. IMPORTANCE The mechanisms through which plant growth-promoting rhizobacteria (PGPR) influence secondary metabolism in perennial crops remain poorly understood. This study demonstrates that Bacillus velezensis SD24, a tea rhizosphere isolate, significantly enhances the accumulation of health-beneficial catechin derivatives in tea leaves. This quality improvement is associated with transcriptionally upregulating key biosynthetic genes ( LAR and ANR ) and concurrently restructuring the rhizosphere microbiome. Furthermore, we reveal a critical antagonistic interaction, where the beneficial fungus Piriformospora indica suppresses these SD24-induced effects. Our findings provide crucial insights into how specific PGPR strains may directly enhance tea quality by affecting host plant metabolism and the root microbiome, highlighting the complex and tailored microbial interactions that could be harnessed for sustainable agriculture.