Plants attacked above-ground by leaf-mining flies change below-ground microbiota to enhance plant defense

Abstract

Root-associated microbiomes play a crucial role in plant responses to biotic and abiotic stresses. Plants can enrich beneficial microbes to increase their stress-relieving ability. Above-ground insect herbivory is among the most detrimental stresses for plants, especially to crop production. However, few studies have explored how root-associated microbiomes respond to herbivores and influence plant-defense functions under herbivory stress. We investigate the changes and functional role of root-associated microbial communities under herbivory stress using leafminer (Liriomyza trifolii) and cowpea (Vigna unguiculata) as a focal system. We did this by using a combination of 16S ribosomal RNA gene profiling and metagenomic sequencing to test for differences in co-occurrence networks and functions between cowpea plants infested and noninfested with leafminers. The results demonstrated that leafminer infestation caused a shift in the rhizosphere microbiome, which was characterized by a significant variation in microbiome community structure and composition, the selection of hub microbes involved in nitrogen (N) metabolism, and functional enrichment related to N metabolism. Notably, nitrogen-fixing bacteria Bradyrhizobium species were actively enriched and selected to be hubs in the rhizosphere. Inoculation with Bradyrhizobium enhanced cowpea performance under leafminer stress and increased protease inhibitor levels to decrease leafminer fitness. Overall, our study characterized the changes of root-associated microbiota between leafminer-infested and noninfested cowpea plants and revealed the mechanisms underlying the rhizosphere microbiome shift that enhance plant performance and defense against herbivory. Our findings provide further support for the notion that plants enrich rhizosphere microbes to counteract aboveground insect herbivores.

Acknowledgements

This work was financially supported by Hainan Province Science and Technology Special Fund (ZDYF2021XDNY302), Hainan Provincial Natural Science Foundation of China (323RC521), Sanya Science and Technology Innovation Project (2022KJCX19), Hainan Special PhD Scientific Research Foundation of Sanya Yazhou Bay Science and Technology City (HSPHDSRF-2022-04-010). We thank Prof. Hongye Li (Zhejiang University) and Ming Zhang (Zhejiang University) for their insightful discussions and Dr Joshua A. Thia (The University of Melbourne) for his effort on reviewing and professional English editing.

Author contributions

Y.G., Z.-R.Z., and Yi.Z. designed the experiments; Y.G., Q.C., Y.H., W.H., and J.G. performed the experiments; Y.G. wrote the manuscript. Z.-R.Z., Yi.Z., Yu.Z., and Q.Y. revised the manuscript.

Data availability

The sequencing raw data have been uploaded to the National Genomics Data Center (https://ngdc.cncb.ac.cn/gsa) [74, 75] with accession number GSA: CRA013220.

Conflict of interest statement

All authors declare that no conflict of interest exists.

Supplementary data

Supplementary data is available at Horticulture Research online.

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