Soil conditions and the plant microbiome boost the accumulation of monoterpenes in the fruit of Citrus reticulata `Chachi'

Background The medicinal material quality of Citrus reticulata `Chachi' differs depending on the bioactive components influenced by the planting area. Environmental factors, such as soil nutrients, the plant-associated microbiome and climatic conditions, play important roles in the accumulation of bioactive components in citrus. However, how these environmental factors mediate the production of bioactive components of medicinal plants remains understudied. Results Here, a multi-omics approach was used to clarify the role of environmental factors such as soil nutrients and the root-associated microbiome on the accumulation of monoterpenes in the peel of C. reticulata `Chachi' procured from core (geo-authentic product region) and non-core (non-geo-authentic product region) geographical regions. The soil environment (high salinity, Mg, Mn and K) enhanced the monoterpene content by promoting the expression of salt stress-responsive genes and terpene backbone synthase in the host plants from the core region. The microbial effects on the monoterpene accumulation of citrus from the core region were further verified by synthetic community (SynCom) experiments. Rhizosphere microorganisms activated terpene synthesis and promoted monoterpene accumulation through interactions with the host immune system. Endophyte microorganisms derived from soil with the potential for terpene synthesis might enhance monoterpene accumulation in citrus by providing precursors of monoterpenes. Conclusions Overall, this study demonstrated that both soil properties and the soil microbiome impacted monoterpene production in citrus peel, thus providing an essential basis for increasing fruit quality via reasonable fertilization and precision microbiota management.

Automated summary

This study used a multi-omics approach to investigate the effects of environmental factors on the accumulation of monoterpenes in citrus peel. It was found that soil nutrients and root-associated microbiome play important roles in the production of monoterpenes. The soil environment, including high salinity and certain nutrients, can enhance monoterpene content in citrus peel by promoting the expression of specific genes. Additionally, interactions between rhizosphere microorganisms and the host immune system can activate terpene synthesis and contribute to monoterpene accumulation.