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

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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.

References

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

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

    Google Scholar 

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

  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).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

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

    Article  Google Scholar 

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

  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).

    Article  PubMed  PubMed Central  Google Scholar 

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

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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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Authors and Affiliations

  1. Department of Plant Pathology, University of California, Davis, CA, USA

    Robert Blundell, Andrea L. Cheung & Clare L. Casteel

  2. Department of Plant Sciences, University of California, Davis, CA, USA

    Jennifer E. Schmidt

  3. Department of Entomology and Nematology, University of California, Davis, CA, USA

    Alexandria Igwe & Rachel L. Vannette

  4. School of Integrative Plant Science, Plant-Microbe Biology and Plant Pathology Section, Cornell University, Ithaca, NY, USA

    Clare L. Casteel

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  1. Robert Blundell
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  2. Jennifer E. Schmidt
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  3. Alexandria Igwe
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  4. Andrea L. Cheung
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  5. Rachel L. Vannette
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  6. Amélie C. M. Gaudin
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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.

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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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