Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

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.

References

  1. 1.

    Verbruggen, E. et al. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol. 186, 968–979 (2010).

    CAS  PubMed  Google Scholar 

  2. 2.

    Lori, M., Symnaczik, S., Mäder, P., De Deyn, G. & Gattinger, A. Organic farming enhances soil microbial abundance and activity—a meta-analysis and meta-regression. PLoS ONE 12, e0180442 (2017).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Lupatini, M., Korthals, G. W., de Hollander, M., Janssens, T. K. S. & Kuramae, E. E. Soil microbiome is more heterogeneous in organic than in conventional farming system. Front. Microbiol. 7, 2064 (2016).

    PubMed  Google Scholar 

  4. 4.

    Gosling, P., Hodge, A., Goodlass, G. & Bending, G. D. Arbuscular mycorrhizal fungi and organic farming. Agric. Ecosyst. Environ. 113, 17–35 (2006).

    Google Scholar 

  5. 5.

    Reganold, J. P. & Wachter, J. M. Organic agriculture in the twenty-first century. Nat. Plants 2, 15221 (2016).

    PubMed  Google Scholar 

  6. 6.

    Shennan, C. et al. Organic and conventional agriculture: a useful framing? Annu. Rev. Environ. Resour. 42, 317–346 (2017).

    Google Scholar 

  7. 7.

    Seufert, V. & Ramankutty, N. Many shades of gray—the context-dependent performance of organic agriculture. Sci. Adv. 3, e1602638 (2017).

    PubMed  PubMed Central  Google Scholar 

  8. 8.

    Crowder, D. W., Northfield, T. D., Strand, M. R. & Snyder, W. E. Organic agriculture promotes evenness and natural pest control. Nature 466, 109–112 (2010).

    CAS  PubMed  Google Scholar 

  9. 9.

    Lichtenberg, E. M. et al. A global synthesis of the effects of diversified farming systems on arthropod diversity within fields and across agricultural landscapes. Glob. Change Biol. 23, 4946–4957 (2017).

    Google Scholar 

  10. 10.

    Muneret, L. et al. Evidence that organic farming promotes pest control. Nat. Sustain. 1, 361–368 (2018).

    Google Scholar 

  11. 11.

    Garratt, M. P. D., Wright, D. J. & Leather, S. R. The effects of farming system and fertilisers on pests and natural enemies: a synthesis of current research. Agric. Ecosyst. Environ. 141, 261–270 (2011).

    Google Scholar 

  12. 12.

    Drinkwater, L., Letourneau, D., Workneh, F., van Bruggen, A. & Shennan, C. Fundamental differences between conventional and organic tomato agroecosystems in California. Ecol. Appl. 5, 1098–1112 (1995).

    Google Scholar 

  13. 13.

    Hole, D. G. et al. Does organic farming benefit biodiversity? Biol. Conserv. 122, 113–130 (2005).

    Google Scholar 

  14. 14.

    Mattson, W. J. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11, 119–161 (1980).

    Google Scholar 

  15. 15.

    Megali, L., Glauser, G. & Rasmann, S. Fertilization with beneficial microorganisms decreases tomato defenses against insect pests. Agron. Sustain. Dev. 34, 649–656 (2014).

    CAS  Google Scholar 

  16. 16.

    Hartmann, M., Frey, B., Mayer, J., Mäder, P. & Widmer, F. Distinct soil microbial diversity under long-term organic and conventional farming. ISME J. 9, 1177–1194 (2015).

    PubMed  Google Scholar 

  17. 17.

    Schmidt, J. E. et al. Effects of Agricultural Management on Rhizosphere Microbial Structure and Function in Processing Tomato Plants. Appl. Environ. Microbiol. 85, e01064-19 (2019).

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Vannette, R. L. & Hunter, M. D. Mycorrhizal fungi as mediators of defence against insect pests in agricultural systems. Agric. Entomol. 11, 351–358 (2009).

    Google Scholar 

  19. 19.

    Pineda, A., Zheng, S.-J., van Loon, J. J. A., Pieterse, C. M. J. & Dicke, M. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15, 507–514 (2010).

    CAS  PubMed  Google Scholar 

  20. 20.

    Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012).

    CAS  PubMed  Google Scholar 

  21. 21.

    Pozo, M. J. & Azcón-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393–398 (2007).

    CAS  PubMed  Google Scholar 

  22. 22.

    Vannette, R. L. & Hunter, M. D. Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. J. Ecol. 99, 66–76 (2010).

    Google Scholar 

  23. 23.

    Fritz, M., Jakobsen, I., Lyngkjær, M. F., Thordal-Christensen, H. & Pons-Kühnemann, J. Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16, 413–419 (2006).

    Google Scholar 

  24. 24.

    Kempel, A., Schmidt, A. K., Brandl, R. & Schädler, M. Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Funct. Ecol. 24, 293–300 (2010).

    Google Scholar 

  25. 25.

    Pineda, A., Kaplan, I. & Bezemer, T. M. Steering soil microbiomes to suppress aboveground insect pests. Trends Plant Sci. 22, 770–778 (2017).

    CAS  PubMed  Google Scholar 

  26. 26.

    Pangesti, N., Pineda, A., Pieterse, C. M. J., Dicke, M. & Van Loon, J. J. A. Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front. Plant Sci. 4, 414 (2013).

    PubMed  PubMed Central  Google Scholar 

  27. 27.

    Katayama, N., Zhang, Z. Q. & Ohgushi, T. Community-wide effects of below-ground rhizobia on above-ground arthropods. Ecol. Entomol. 36, 43–51 (2011).

    Google Scholar 

  28. 28.

    De Souza, R., Ambrosini, A. & Passaglia, L. M. P. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet. Mol. Biol. 38, 401–419 (2015).

    PubMed  PubMed Central  Google Scholar 

  29. 29.

    Chen, L.-F., Batuman, O., Aegerter, B. J., Willems, J. & Gilbertson, R. L. First report of curly top disease of pepper and tomato in California caused by the spinach curly top strain of beet curly top virus. Plant Dis. 101, 1334 (2017).

    Google Scholar 

  30. 30.

    Erb, M., Meldau, S. & Howe, G. A. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17, 250–259 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Bari, R. & Jones, J. D. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69, 473–488 (2009).

    CAS  PubMed  Google Scholar 

  32. 32.

    Prudic, K. L., Oliver, J. C. & Bowers, M. D. Soil nutrient effects on oviposition preference, larval performance, and chemical defense of a specialist insect herbivore. Oecologia 143, 578–587 (2005).

    PubMed  Google Scholar 

  33. 33.

    Lu, Z., Yu, X., Heong, K. & Hu, C. Effect of nitrogen fertilizer on herbivores and its stimulation to major insect pests in rice. Rice Sci. 14, 56–66 (2007).

    Google Scholar 

  34. 34.

    Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).

    CAS  PubMed  Google Scholar 

  35. 35.

    Wolf, K. M. et al. The century experiment: the first twenty years of UC Davis’ Mediterranean agroecological experiment. Ecology 99, 503 (2018).

    PubMed  Google Scholar 

  36. 36.

    Walling, L. L. Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146, 859–866 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Kaloshian, I. & Walling, L. L. Hemipterans as plant pathogens. Annu. Rev. Phytopathol. 43, 491–521 (2005).

    CAS  PubMed  Google Scholar 

  38. 38.

    Rodríguez-Álvarez, C., López-Climent, M. F., Gómez-Cadenas, A., Kaloshian, I. & Nombela, G. Salicylic acid is required for Mi-1-mediated resistance of tomato to whitefly Bemisia tabaci, but not for basal defense to this insect pest. Bull. Entomol. Res. 105, 574–582 (2015).

    PubMed  Google Scholar 

  39. 39.

    Ellis, C., Karafyllidis, L. & Turner, J. G. Constitutive activation of jasmonate signaling in an Arabidopsis mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Mol. Plant–Microbe Interact. 15, 1025–1030 (2002).

    CAS  PubMed  Google Scholar 

  40. 40.

    Kloth, K. J. et al. AtWRKY22 promotes susceptibility to aphids and modulates salicylic acid and jasmonic acid signalling. J. Exp. Bot. 67, 3383–3396 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Cui, J. et al. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc. Natl Acad. Sci. USA 102, 1791–1796 (2005).

    CAS  PubMed  Google Scholar 

  42. 42.

    Barber, N. A., Kiers, E. T., Theis, N., Hazzard, R. V. & Adler, L. S. Linking agricultural practices, mycorrhizal fungi, and traits mediating plant–insect interactions. Ecol. Appl. 23, 1519–1530 (2013).

    PubMed  Google Scholar 

  43. 43.

    Nakano, M. & Mukaihara, T. Ralstonia solanacearum type III effector RipAL targets chloroplasts and induces jasmonic acid production to suppress salicylic acid-mediated defense responses in plants. Plant Cell Physiol. 59, 2576–2589 (2018).

    CAS  PubMed  Google Scholar 

  44. 44.

    Baichoo, Z. & Jaufeerally-Fakim, Y. Ralstonia solanacearum upregulates marker genes of the salicylic acid and ethylene signaling pathways but not those of the jasmonic acid pathway in leaflets of Solanum lines during early stage of infection. Eur. J. Plant Pathol. 147, 615–625 (2017).

    CAS  Google Scholar 

  45. 45.

    Berg, M. & Koskella, B. Nutrient- and dose-dependent microbiome-mediated protection against a plant pathogen. Curr. Biol. 28, 2487–2492 (2018).

    CAS  PubMed  Google Scholar 

  46. 46.

    Blubaugh, C. K., Carpenter-Boggs, L., Reganold, J. P., Schaeffer, R. N. & Snyder, W. E. Bacteria and competing herbivores weaken top-down and bottom-up aphid suppression. Front. Plant Sci. 9, 1239 (2018).

    PubMed  PubMed Central  Google Scholar 

  47. 47.

    Heinen, R. et al. Species-specific plant–soil feedbacks alter herbivore-induced gene expression and defense chemistry in Plantago lanceolata. Oecologia 188, 801–811 (2018).

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Bastías, D. A. et al. Jasmonic acid regulation of the anti-herbivory mechanism conferred by fungal endophytes in grasses. J. Ecol. 106, 2365–2379 (2018).

    Google Scholar 

  49. 49.

    Gilbert, L. & Johnson, D. Plant-mediated ‘apparent effects’ between mycorrhiza and insect herbivores. Curr. Opin. Plant Biol. 26, 100–105 (2015).

    PubMed  Google Scholar 

  50. 50.

    Howard, M. M., Kao-Kniffin, J. & Kessler, A. Shifts in plant–microbe interactions over community succession and their effects on plant resistance to herbivores. New Phytol. 226, 1144–1157 (2020).

    PubMed  Google Scholar 

  51. 51.

    Brading, P. A., Hammond-Kosack, K. E., Parr, A. & Jones, J. D. G. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J. 23, 305–318 (2000).

    CAS  PubMed  Google Scholar 

  52. 52.

    Lightner, J., Pearce, G., Ryan, C. A. & Browse, J. Isoaltion of signalling mutants of tomato (Lycopersicon esculentum). Mol. Genet. Genomics 241, 595–601 (1993).

    Google Scholar 

  53. 53.

    Casteel, C. L. et al. Disruption of ethylene responses by turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol. 169, 209–218 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Microchemical Determination of Carbon, Hydrogen, and Nitrogen AOAC 972.43-1975 (AOAC Official Method, 2006).

  55. 55.

    Knepel, K. Determination of nitrate in 2M KCl soil extracts by flow injection analysis. QuikChem Method 12, 107 (2003).

    Google Scholar 

  56. 56.

    Olsen, S. R. & Sommers, L. E. in Methods of Soil Analysis. Part 2 Chemical and Microbiological Properties 2nd edn (eds Page, A. et al.) 403–427 (ASA and SSSA, 1982).

  57. 57.

    Nelson, D.W. & Sommers, L.E. in Methods of Soil Analysis. Part 3. Chemical Methods (eds Sparks, D. L. et al.) 961–1010 (SSSA and ASA, 1996).

  58. 58.

    Jones, J.B. Laboratory Guide for Conducting Soil Tests and Plant Analysis (CRC Press, 2001).

  59. 59.

    Walters, W. et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems 1, e00009-15 (2016).

    PubMed  Google Scholar 

  60. 60.

    Callahan, B. J. et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Glöckner, F. O. et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J. Biotechnol. 261, 169–176 (2017).

    PubMed  Google Scholar 

  62. 62.

    Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).

    PubMed  Google Scholar 

  63. 63.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).

  64. 64.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

  65. 65.

    Oksanen, J. et al. VEGAN: Community Ecology Package v.2.5-4 (2018).

  66. 66.

    Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550–571 (2014).

    PubMed  PubMed Central  Google Scholar 

  67. 67.

    RStudio Team RStudio: Integrated Development for R v.1.0.136 (2015).

Download references

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.

Author information

Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Clare L. Casteel.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplemental Information

Supplementary Tables 1–5 and Figs. 1–3.

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing