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Organic management promotes natural pest control through altered plant resistance to insects

Abstract

Reduced insect pest populations found on long-term organic farms have mostly been attributed to increased biodiversity and abundance of beneficial predators, as well as to changes in plant nutrient content. However, the role of plant resistance has largely been ignored. Here, we determine whether host plant resistance mediates decreased pest populations in organic systems and identify potential underpinning mechanisms. We demonstrate that fewer numbers of leafhoppers (Circulifer tenellus) settle on tomatoes (Solanum lycopersicum) grown using organic management as compared to conventional. We present multiple lines of evidence, including rhizosphere soil microbiome sequencing, chemical analysis and transgenic approaches, to demonstrate that changes in leafhopper settling between organically and conventionally grown tomatoes are dependent on salicylic acid accumulation in plants and mediated by rhizosphere microbial communities. These results suggest that organically managed soils and microbial communities may play an unappreciated role in reducing plant attractiveness to pests by increasing plant resistance.

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Fig. 1: Organic management practices reduced insect settling and altered plant defence signalling pathways.
Fig. 2: Bacterial and fungal diversity and community composition differ among organic and conventional sites.
Fig. 3: Relative abundance of bacterial orders associated with changes in SA.
Fig. 4: Soil biota drives differences in leafhopper populations, preference and plant resistance.
Fig. 5: Soil biota drive differences in hemipteran population growth across plant species.

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Data availability

All data that support these findings are available from C.L.C., A.G. and R.L.V. upon request. The raw sequencing dataset is available at the NCBI SRA data repository under the project accession number PRJNA539989.

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Acknowledgements

We thank F. Bender, J. Richardy, G. Hall, S. Tookey, University of California Cooperative Extension (UCCE) farm advisors, Russell Ranch staff and growers for participating in this study and assisting with sampling. This work was supported by start-up funds from UC Davis to C.L.C., A.G. and R.L.V.; the California Tomato Research Institute to A.G., C.L.C. and R.L.V.; the California Potato Research Advisory Board to C.L.C. and the USDA-NIFA, Agricultural Experiment Station Projects no. CA-D-PPA-2297-H to C.L.C., no. CA-D-PLS-2332-H to A.G. and no. CA-D-ENM-2354-RR to R.L.V.

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R.B., A.L.C., J.E.S, C.L.C, R.L.V. and A.I. conducted most of the experiments and analysis. C.L.C., A.G. and R.L.V. designed all experiments and directed the project. R.B., C.L.C., A.G. and R.L.V. wrote the paper with comments and input from all authors.

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Correspondence to Clare L. Casteel.

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Blundell, R., Schmidt, J.E., Igwe, A. et al. Organic management promotes natural pest control through altered plant resistance to insects. Nat. Plants 6, 483–491 (2020). https://doi.org/10.1038/s41477-020-0656-9

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