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Enhanced agricultural sustainability through within-species diversification

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Abstract

Agriculture has played an important role in human health and welfare by producing large amounts of food to feed a growing world population, but this has also placed substantial pressures on natural resources and the environment. One of the most pressing challenges in agriculture is how to ensure food security and promote long-term social-economic development while maintaining healthy, sustainable ecosystems capable of quickly adapting to changing environments. Previous studies demonstrated the positive impact of mixed planting strategies on crop productivity as a consequence of reduced disease impact. Here we present data from a series of trials involving within-species diversification of potatoes grown under smallholding conditions, showing that the benefits of mixed planting strategies extend beyond increases in yield, production resilience and reductions in disease, to increased soil microbial diversity, improved soil nutrients and reduced evolution in the associated Phytophthora infestans pathogen. Taken together, these synergistic benefits provide a good opportunity for achieving sustainable agriculture.

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Fig. 1: Impacts of host diversity on crop yields.
Fig. 2: Impact of host diversity on disease epidemics.
Fig. 3: Impact of host diversity on different measurements of soil fertility.
Fig. 4: Impact of host diversity on pathogen evolution and aggressiveness.
Fig. 5: Impact of host diversity on pathogen diversity.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Burdon, J. J., Barrett, L. G., Rebetzke, G. & Thrall, P. H. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 7, 609–624 (2014).

    Article  Google Scholar 

  2. Zhan, J., Thrall, P. H., Papaïx, J., Xie, L. & Burdon, J. J. Playing on a pathogen’s weakness: using evolution to guide sustainable plant disease control strategies. Annu. Rev. Phytopathol. 53, 19–43 (2015).

    CAS  Article  Google Scholar 

  3. Garrett, K. A. & Mundt, C. C. Host diversity can reduce potato late blight severity for focal and general patterns of primary inoculum. Phytopathology 90, 1307–1312 (2000).

    CAS  Article  Google Scholar 

  4. Newton, A. C., Ellis, R. P., Hackett, C. A. & Guy, D. C. The effect of component number on Rhynchosporium secalis infection and yield in mixtures of winter barley cultivars. Plant Pathol. 45, 930–938 (1997).

    Article  Google Scholar 

  5. Zhu, Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).

    CAS  Article  Google Scholar 

  6. Carson, M. L. Crown rust development and selection for virulence in Puccinia coronata f. sp. avenae in an oat multiline cultivar. Plant Dis. 93, 347–353 (2009).

    Article  Google Scholar 

  7. Mundt, C. C., Sackett, K. E. & Wallace, L. D. Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. Ecol. Appl. 21, 321–328 (2011).

    Article  Google Scholar 

  8. Newton, A. C. et al. Soil tillage effects on the efficacy of cultivars and their mixtures in winter barley. Field Crop. Res. 128, 91–100 (2012).

    Article  Google Scholar 

  9. Doring, T. F. et al. Comparative analysis of performance and stability among composite cross populations, variety mixtures and pure lines of winter wheat in organic and conventional cropping systems. Field Crop. Res. 183, 2345–245 (2015).

    Google Scholar 

  10. Cook, R. J. & Veseth, R. J. Wheat Health Management (American Phytopathological Society, St. Paul, 1991).

    Google Scholar 

  11. Smithson, J. B. & Lenne, J. M. Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Ann. Appl. Biol. 128, 127–158 (1996).

    Article  Google Scholar 

  12. Mundt, C. C. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381–410 (2002).

    CAS  Article  Google Scholar 

  13. Creissen, H. E., Jorgensen, T. H. & Brown, J. K. Increased yield stability of field-grown winter barley (Hordeum vulgare L.) varietal mixtures through ecological processes. Crop. Prot. 85, 1–8 (2016).

    Article  Google Scholar 

  14. Sommerhalder, R. J., McDonald, B. A., Mascher, F. & Zhan, J. Effect of hosts on competition among clones and evidence of differential selection between pathogenic and saprophytic phases in experimental populations of the wheat pathogen Phaeosphaeria nodorum. BMC Evol. Biol. 11, 188 (2011).

    Article  Google Scholar 

  15. Zhan, J., Mundt, C. C., Hoffer, M. E. & McDonald, B. A. Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem. J. Evol. Biol. 15, 634–647 (2002).

    Article  Google Scholar 

  16. Chin, K. M. & Wolfe, M. S. Selection on Erysiphe graminis in pure and mixed stands of barley. Plant Pathol. 33, 535–546 (1984).

    Article  Google Scholar 

  17. Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl Acad. Sci. USA 70, 3321–3323 (1973).

    CAS  Article  Google Scholar 

  18. Wricke, G. Cinc mehtodo zer ertussog der okojogischen streobrelte in Felder. Versochen Z. Oflanzenzucht 47, 92–96 (1962).

    Google Scholar 

  19. Finckh, M. et al. Cereal variety and species mixtures in practice, with emphasis on disease resistance. Agronomie 20, 813–837 (2000).

    Article  Google Scholar 

  20. Cowger, C. & Mundt, C. C. Effects of wheat cultivar mixtures on epidemic progression of septoria tritici blotch and pathogenicity of Mycosphaerella graminicola. Phytopathology 92, 617–623 (2002).

    Article  Google Scholar 

  21. Cox, C. M. et al. Cultivar mixtures for the simultaneous management of multiple diseases: tan spot and leaf rust of wheat. Phytopathology 94, 961–969 (2004).

    CAS  Article  Google Scholar 

  22. Skelsey, P. et al. Influence of host diversity on development of epidemics: an evaluation and elaboration of mixture theory. Phytopathology 95, 328–338 (2005).

    CAS  Article  Google Scholar 

  23. Andrivon, D., Lucas, J. M. & Ellisseche, D. Development of natural late blight epidemics in pure and mixed plots of potato cultivars with different levels of partial resistance. Plant Pathology 52, 586–594 (2003).

    Article  Google Scholar 

  24. Garrett, K. A. et al. The effects of host diversity and other management components on epidemics of potato late blight in the humid highland tropics. Phytopathology 91, 993–1000 (2001).

    CAS  Article  Google Scholar 

  25. Phillips, S. L., Shaw, M. W. & Wolfe, M. S. The effect of potato variety mixtures on epidemics of late blight, in relation to plot size and level of resistance. Ann. Appl. Biol. 147, 245–252 (2005).

    Article  Google Scholar 

  26. Loreau, M. & Hector, A. Partitioning selection and complementarity in biodiversity experiments. Science 412, 72–76 (2001).

    CAS  Google Scholar 

  27. Tilman, D. et al. Diversity and productivity in a long-term grassland experiment. Science 294, 843–845 (2001).

    CAS  Article  Google Scholar 

  28. Zak, D. R. et al. Plant diversity, soil microbial communities and ecosystem function: are there any links? Ecology 84, 2042–2050 (2003).

    Article  Google Scholar 

  29. Dybzinski, R. et al. Soil fertility increases with plant species diversity in a long-term biodiversity experiment. Oecologia. 158, 85–93 (2008).

    Article  Google Scholar 

  30. Richardson, A. E. & Simpson, R. J. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol. 156, 989–996 (2011).

    CAS  Article  Google Scholar 

  31. Yang, G. et al. The interaction between arbuscular mycorrhizal fungi and soil phosphorus availability influences plant community productivity and ecosystem stability. J. Ecol. 102, 1072–1082 (2014).

    CAS  Article  Google Scholar 

  32. Jacoby, R. et al. The role of soil microorganisms in plant mineral nutrition—current knowledge and future directions. Trends. Plant. Sci. 8, 1617 (2017).

    Google Scholar 

  33. Smith, S. E., Smith, F. A. & Jakobsen, I. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 133, 16–20 (2003).

    CAS  Article  Google Scholar 

  34. Tkacz, A. & Poole, P. Role of root microbiota in plant productivity. J. Exp. Botany 66, 2167–2175 (2015).

    CAS  Article  Google Scholar 

  35. Liu, Z., Liu, G. H., Fu, B. J. & Zheng, X. Relationship between plant species diversity and soil microbial functional diversity along a longitudinal gradient in temperate grasslands of Hulunbeir, Inner Mongolia, China. Ecol. Res. 23, 511–518 (2008).

    Article  Google Scholar 

  36. Berg, G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Bio. 84, 11–18 (2009).

    CAS  Article  Google Scholar 

  37. Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 8413 (2015).

    CAS  Article  Google Scholar 

  38. Lambers, H., Mougel, C., Jaillard, B. & Hinsinger, P. Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321, 83–115 (2009).

    CAS  Article  Google Scholar 

  39. Heather, L. et al. Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 83, 2281–2291 (2003).

    Google Scholar 

  40. Garrett, K. A. et al. Intraspecific functional diversity in hosts and its effect on disease risk across a climatic gradient. Ecol. Appl. 19, 1868–1883 (2009).

    CAS  Article  Google Scholar 

  41. Zhu, W. et al. Increased frequency of self-fertile isolates in Phytophthora infestans may attribute to their higher fitness relative to the A1 isolates. Sci. Rep. 6, 29428 (2016).

    CAS  Article  Google Scholar 

  42. Yang, L. et al. Trade-offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans. Mol. Ecol. 25, 4047–4058 (2016).

    Article  Google Scholar 

  43. Abang, M. et al. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 96, 1214–1222 (1996).

    Article  Google Scholar 

  44. Marshall, B., Newton, A. C. & Zhan, J. Quantitative evolution of aggressiveness of powdery mildew in a two cultivar barley mixture. Plant Pathol. 58, 378–388 (2009).

    Article  Google Scholar 

  45. Lannou, C. & Mundt, C. C. Evolution of a pathogen population in host mixtures: rate of emergence of complex races. Theor. Appl. Genet. 94, 991–999 (1997).

    Article  Google Scholar 

  46. Black, W., Mastenbroek, C., Mills, W. R. & Peterson, L. C. A proposal for an international nomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivatives. Euphytica 2, 173–179 (1953).

    Article  Google Scholar 

  47. Burdon, J. J., Zhan, J., Barrett, L. G., Papaïx, J. & Thrall, P. H. Addressing the challenges of pathogen evolution on the world’s arable crops. Phytopathology 106, 1117–1127 (2016).

    CAS  Article  Google Scholar 

  48. Zhan, J. & McDonald, B. A. Experimental measures of pathogen competition and relative fitness. Annu.Rev. Phytopathol. 51, 131–153 (2013).

    CAS  Article  Google Scholar 

  49. Zhan, J. et al. Achieving sustainable plant disease management through evolutionary principles. Trends. Plant. Sci. 19, 570–575 (2014).

    CAS  Article  Google Scholar 

  50. Wang, B. et al. Potato viruses in China. Crop. Prot. 30, 1117–1123 (2011).

    Article  Google Scholar 

  51. Wu, E. et al. Diverse mechanisms shape the evolution of virulence factors in the potato late blight pathogen Phytophthora infestans sampled from China. Sci. Rep. 6, srep26182 (2016).

    Article  Google Scholar 

  52. Zhu, W. et al. Limited sexual reproduction and quick turnover in the population genetic structure of Phytophthora infestans in Fujian, China. Sci. Rep. 5, 10094 (2015).

    CAS  Article  Google Scholar 

  53. Qin, C. et al. Comparative analyses of fungicide sensitivity and SSR marker variations indicate a low risk of developing azoxystrobin resistance in Phytophthora infestans. Sci. Rep. 6, 20483 (2016).

    CAS  Article  Google Scholar 

  54. Lees, A. K. et al. Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathol. 55, 311–319 (2006).

    CAS  Article  Google Scholar 

  55. Armstrong, M. R. et al. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl Acad. Sci. USA 102, 7766–7771 (2005).

    CAS  Article  Google Scholar 

  56. Chen, Y. & Halterman, D. A. Phenotypic characterization of potato late blight resistance mediated by the broad-spectrum resistance gene RB. Phytopathology 101, 263–270 (2011).

    CAS  Article  Google Scholar 

  57. Zhu, S. et al. An updated conventional- and a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans. Euphytica 202, 219–234 (2015).

    Article  Google Scholar 

  58. Garland, J. L. & Mills, A. L. Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl. Environ. Microb. 57, 2351–2359 (1991).

    CAS  Google Scholar 

  59. Barrow, N. J. Soil phosphate chemistry and the P-sparing effect of previous phosphate applications. Plant Soil 397, 401–409 (2015).

    CAS  Article  Google Scholar 

  60. Walia, M. K. & Dick, W. A. Soil chemistry and nutrient concentrations in perennial ryegrass as influenced by gypsum and carbon amendments. J. Soil Sci. Plant Nut. 16, 832–847 (2016).

    CAS  Google Scholar 

  61. Ertiftik, H. & Zengin, M. Response of maize for grain to potassium and magnesium fertilizers in soils with high lime contents. J. Plant Nutr. 40, 98–103 (2017).

    Article  Google Scholar 

  62. Jeger, M. J. & Viljanen-Rollinson, S. The use of the area under the disease-progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor. Appl. Genet. 102, 32–40 (2001).

    Article  Google Scholar 

  63. Zak, J. C., Willig, M. R., Moorhead, D. L. & Wildman, H. G. Functional diversity of microbial communities: a quantitative approach. Soil Biol. Biochem. 26, 1101–1108 (1994).

    Article  Google Scholar 

  64. Everitt, B. S The Analysis of Contingency Tables. 2nd edn (Chapman & Hall/CRC Press: Boca Raton, 1992).

    Google Scholar 

  65. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011).

    CAS  Article  Google Scholar 

  66. Librado, P. & Rozas, J. DnaSPv5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452 (2009).

    CAS  Article  Google Scholar 

  67. Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–426 (1986).

    CAS  Google Scholar 

  68. Lawrence, I. & Lin, K. A concordance correlation coefficient to evaluate reproducibility. Biometrics 45, 255–268 (1989).

    Article  Google Scholar 

  69. Ott, R. L. An Introduction to Statistical Methods and Data Analysis 5th edn (Duxbury Press, Belmont, 1992).

    Google Scholar 

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Acknowledgements

This work was supported by National Natural Science Foundation of China (grant Nos. U1405213, 31761143010 and 31460368) and the China Agriculture Research System (No. CARS-09-P20).

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Authors

Contributions

L.N.Y. collected and genotyped pathogen isolates, generated sequence and pathogenicity data, analysed data and wrote the manuscript. Z.C.P. conducted field experiments, generated soil nutrition and microbial data and wrote the manuscript. W.Z and E.J.W. collected pathogen isolates, generated sequence and pathogenicity data and wrote the manuscript. D.C.H., X.Y., Y.Y.Q. and Y.W. conducted field experiments, collected pathogen isolates and pathogenicity data. R.S.C., L.P.S., P.H.T. and J.J.B. wrote the manuscript. Q.J.S. conceived and supervised the experiments. J.Z. conceived, designed and supervised the experiments, analysed the data and wrote the manuscript. All authors reviewed the manuscript.

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Correspondence to Qi-Jun Sui or Jiasui Zhan.

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Supplementary Tables 1–2, Supplementary Figures 1–3

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Yang, LN., Pan, ZC., Zhu, W. et al. Enhanced agricultural sustainability through within-species diversification. Nat Sustain 2, 46–52 (2019). https://doi.org/10.1038/s41893-018-0201-2

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