Diversity and interactions of rhizobacteria determine multinutrient traits in tomato host plants under nitrogen and water disturbances

Abstract

Coevolution within the plant holobiont extends the capacity of host plants for nutrient acquisition and stress resistance. However, the role of the rhizospheric microbiota in maintaining multinutrient utilization (i.e. multinutrient traits) in the host remains to be elucidated. Multinutrient cycling index (MNC), analogous to the widely used multifunctionality index, provides a straightforward and interpretable measure of the multinutrient traits in host plants. Using tomato as a model plant, we characterized MNC (based on multiple aboveground nutrient contents) in host plants under different nitrogen and water supply regimes and explored the associations between rhizospheric bacterial community assemblages and host plant multinutrient profiles. Rhizosphere bacterial community diversity, quantitative abundance, predicted function, and key topological features of the co-occurrence network were more sensitive to water supply than to nitrogen supply. A core bacteriome comprising 61 genera, such as Candidatus Koribacter and Streptomyces, persisted across different habitats and served as a key predictor of host plant nutrient uptake. The MNC index increased with greater diversity and higher core taxon abundance in the rhizobacterial community, while decreasing with higher average degree and graph density of rhizobacterial co-occurrence network. Multinutrient absorption by host plants was primarily regulated by community diversity and rhizobacterial network complexity under the interaction of nitrogen and water. The high biodiversity and complex species interactions of the rhizospheric bacteriome play crucial roles in host plant performance. This study supports the development of rhizosphere microbiome engineering, facilitating effective manipulation of the microbiome for enhanced plant benefits, which supports sustainable agricultural practices and plant health.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32202468, 32372808), the Basic and Applied Basic Research Foundation of Guangdong Province (2021A1515110126, 2023A1515012213), the Shenzhen Science and Technology Program (202206193000001, 20220816113416001, JCYJ20230807111217035) and the Young Elite Scientists Sponsorship Program by CAST (2019QNRC001). We thank Editage for English language editing.

Author contributions

R.X. and J.G. designed the study. W.S. and X.Y. carried out the experiment. X.Y., Z.L., B.W., and D.W. collected data and samples. W.S. wrote the initial draft of the manuscript. J.G., R.X., S.S., Y.S., and J.T. made valuable comments on the manuscript.

Data availability

All the raw sequence data were submitted to the NCBI Sequence Read Archive (SRA) database under accession no. PRJNA1042797.

Conflict of interest statement

The authors declare no competing interests.

Supplementary Data

Supplementary data is available at Horticulture Research online.

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