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A plant biodiversity effect resolved to a single chromosomal region

Nature Ecology & Evolution volume 2, pages 1933–1939 (2018)Cite this article

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Abstract

Despite extensive evidence that biodiversity promotes plant community productivity, progress towards understanding the mechanistic basis of this effect remains slow, impeding the development of predictive ecological theory and agricultural applications. Here, we analysed non-additive interactions between genetically divergent Arabidopsis accessions in experimental plant communities. By combining methods from ecology and quantitative genetics, we identify a major effect locus at which allelic differences between individuals increase the above-ground productivity of communities. In experiments with near-isogenic lines, we show that this diversity effect acts independently of other genomic regions and can be resolved to a single region representing less than 0.3% of the genome. Using plant–soil feedback experiments, we also demonstrate that allelic diversity causes genotype-specific soil legacy responses in a consecutive growing period, even after the original community has disappeared. Our work thus suggests that positive diversity effects can be linked to single Mendelian factors, and that a range of complex community properties can have a simple cause. This may pave the way to novel breeding strategies, focusing on phenotypic properties that manifest themselves beyond isolated individuals; that is, at a higher level of biological organization.

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Fig. 1: Combining ecological concepts and genetic methods.
Fig. 2: Allelic diversity at a major effect locus increases community productivity.
Fig. 3: Resolving soil × allelic diversity interactions to a single Mendelian factor.
Fig. 4: Allelic diversity effects persist across a generation through their soil legacy.

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Data availability

The datasets described in this paper and a functional annotation of the 86 genes within the fine-mapped diversity QTL are available through the Zenodo data repository (https://doi.org/10.5281/zenodo.1254563). Sequencing data are deposited in the NCBI Sequence Read Archive (accession SRP149077). Analysis scripts are available from the authors on request.

References

  1. Cardinale, B. J. et al. The functional role of producer diversity in ecosystems. Am. J. Bot. 98, 572–592 (2011).

    Article  Google Scholar 

  2. O’Connor, M. I. et al. A general biodiversity–function relationship is mediated by trophic level. Oikos 126, 18–31 (2017).

    Article  Google Scholar 

  3. Cardinale, B. J., Palmer, M. A. & Collins, S. L. Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415, 426–429 (2002).

    Article  CAS  Google Scholar 

  4. Schnitzer, S. A. et al. Soil microbes drive the classic plant diversity–productivity pattern. Ecology 92, 296–303 (2011).

    Article  Google Scholar 

  5. Maron, J. L., Marler, M., Klironomos, J. N. & Cleveland, C. C. Soil fungal pathogens and the relationship between plant diversity and productivity. Ecol. Lett. 14, 36–41 (2011).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Ratcliffe, S. et al. Biodiversity and ecosystem functioning relations in European forests depend on environmental context. Ecol. Lett. 20, 1414–1426 (2017).

    Article  Google Scholar 

  8. Tylianakis, J. M. et al. Resource heterogeneity moderates the biodiversity–function relationship in real world ecosystems. PLoS Biol. 6, 947–956 (2008).

    CAS  Google Scholar 

  9. Flynn, D. F. B., Mirotchnick, N., Jain, M., Palmer, M. I. & Naeem, S. Functional and phylogenetic diversity as predictors of biodiversity—ecosystem–function relationships. Ecology 92, 1573–1581 (2011).

    Article  Google Scholar 

  10. Wright, I. J. et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004).

    Article  CAS  Google Scholar 

  11. Díaz, S. et al. The global spectrum of plant form and function. Nature 529, 167–171 (2015).

    Article  Google Scholar 

  12. Cadotte, M. W., Cardinale, B. J. & Oakley, T. H. Evolutionary history and the effect of biodiversity on plant productivity. Proc. Natl Acad. Sci. USA 105, 17012–17017 (2008).

    Article  CAS  Google Scholar 

  13. Crutsinger, G. M. et al. Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313, 966–968 (2006).

    Article  CAS  Google Scholar 

  14. Wang, S. & Loreau, M. Ecosystem stability in space: α, β and γ variability. Ecol. Lett. 17, 891–901 (2014).

    Article  Google Scholar 

  15. Oehri, J., Schmid, B., Schaepman-Strub, G. & Niklaus, P. A. Biodiversity promotes primary productivity and growing season lengthening at the landscape scale. Proc. Natl Acad. Sci. USA 38, 10160–10165 (2017).

    Article  Google Scholar 

  16. Siefert, A. et al. A global meta-analysis of the relative extent of intraspecific trait variation in plant communities. Ecol. Lett. 18, 1406–1419 (2015).

    Article  Google Scholar 

  17. Crutsinger, G. M., Souza, L. & Sanders, N. J. Intraspecific diversity and dominant genotypes resist plant invasions. Ecol. Lett. 11, 16–23 (2008).

    PubMed  Google Scholar 

  18. Prieto, I. et al. Complementary effects of species and genetic diversity on productivity and stability of sown grasslands. Nat. Plants 1, 15033 (2015).

    Article  CAS  Google Scholar 

  19. Mendel, G. Versuche über Pflanzenhybriden. Verhandlungen des Naturforschenden Vereines Brünn IV, 3–47 (1865).

  20. Loudet, O., Chaillou, S., Camilleri, C., Bouchez, D. & Daniel-Vedele, F. Bay-0 × Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. Theor. Appl. Genet. 104, 1173–1184 (2002).

    Article  CAS  Google Scholar 

  21. Griffing, B. Concept of general and specific combining ability in relation to diallel crossing systems. Aust. J. Biol. Sci. 9, 463–493 (1956).

    Article  Google Scholar 

  22. Griffing, B. Genetic analysis of plant mixtures. Genetics 122, 943–956 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Zak, D. R., Holmes, W. E., White, D. C., Peacock, A. D. & Tilman, D. Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84, 2042–2050 (2003).

    Article  Google Scholar 

  24. Bukowski, A. R. & Petermann, J. S. Intraspecific plant–soil feedback and intraspecific overyielding in Arabidopsis thaliana. Ecol. Evol. 4, 2533–2545 (2014).

    Article  Google Scholar 

  25. Meyer, S. T. et al. Effects of biodiversity strengthen over time as ecosystem functioning declines at low and increases at high biodiversity. Ecosphere 7, e01619 (2016).

    Article  Google Scholar 

  26. Clements, F. E. & Goldsmith, G. W. The Phytometer Method in Ecology (Carnegie Institution of Washington, Washington DC, 1924).

  27. Dawkins, R. The Extended Phenotype (Oxford Univ. Press, Oxford, 1982).

  28. MacKay, T. F. C., Stone, E. A. & Ayroles, J. F. The genetics of quantitative traits: challenges and prospects. Nat. Rev. Genet. 10, 565–577 (2009).

    Article  CAS  Google Scholar 

  29. Boyle, E. A., Li, Y. I. & Pritchard, J. K. An expanded view of complex traits: from polygenic to omnigenic. Cell 169, 1177–1186 (2017).

    Article  CAS  Google Scholar 

  30. Wilfert, L. & Schmid-Hempel, P. The genetic architecture of susceptibility to parasites. BMC Evol. Biol. 8, 187 (2008).

    Article  Google Scholar 

  31. Wittwer, R. A., Dorn, B., Jossi, W. & Van Der Heijden, M. G. A. Cover crops support ecological intensification of arable cropping systems. Sci. Rep. 7, 41911 (2017).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Litrico, I. & Violle, C. Diversity in plant breeding: a new conceptual framework. Trends Plant Sci. 20, 604–613 (2015).

    Article  CAS  Google Scholar 

  35. Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).

    Article  CAS  Google Scholar 

  36. Edgerton, M. D. Increasing crop productivity to meet global needs for feed, food, and fuel. Plant Physiol. 149, 7–13 (2009).

    Article  CAS  Google Scholar 

  37. Lippman, Z. B. & Zamir, D. Heterosis: revisiting the magic. Trends Genet. 23, 60–66 (2007).

    Article  CAS  Google Scholar 

  38. Weiner, J., Du, Y. L., Zhang, C., Qin, X. L. & Li, F. M. Evolutionary agroecology: individual fitness and population yield in wheat (Triticum aestivum). Ecology 98, 2261–2266 (2017).

    Article  Google Scholar 

  39. Easlon, H. M. & Bloom, A. J. Easy leaf area: automated digital image analysis for rapid and accurate measurement of leaf area. Appl. Plant Sci. 2, apps.1400033 (2014).

    Article  Google Scholar 

  40. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  Google Scholar 

  41. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    Article  Google Scholar 

  42. R Core Development Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2017).

  43. Xie, W. et al. Parent-independent genotyping for constructing an ultrahigh-density linkage map based on population sequencing. Proc. Natl Acad. Sci. USA 107, 10578–10583 (2010).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank B. Schmid and U. Grossniklaus for helpful discussions and sharing infrastructure. We thank J. Bacompte and J. Weiner for helpful comments on the manuscript. We further acknowledge M. Philipp for technical support, E. De Luca and N. Ponta for help with plant measurements, and M. Furler and D. Topalovic for technical greenhouse support. This work was supported by an Ambizione Fellowship (PZ00P3_148223) of the Swiss National Science Foundation (to S.E.W.). P.A.N. acknowledges support from the University of Zurich Priority Program ‘Global Change and Biodiversity’. S.E.W. was also financially supported by funds from the University of Zurich and European Research Council (to U. Grossniklaus).

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Author notes

  1. Samuel E. Wuest

    Present address: Research Division Plant Breeding, Agroscope, Wädenswil, Switzerland

Authors and Affiliations

  1. Department of Plant and Microbial Biology, University of Zurich, Zurich, Switzerland

    Samuel E. Wuest

  2. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

    Pascal A. Niklaus

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  1. Samuel E. Wuest
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  2. Pascal A. Niklaus
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Contributions

S.E.W. conceptualized and designed the research (with input from P.A.N.), and performed the experiments. Both authors performed the analyses and wrote the manuscript. Both authors revised and approved the final version of the manuscript.

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Correspondence to Samuel E. Wuest.

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Supplementary Tables 1–2, Supplementary Figures 1–6, Supplementary Discussion and Supplementary References

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Wuest, S.E., Niklaus, P.A. A plant biodiversity effect resolved to a single chromosomal region. Nat Ecol Evol 2, 1933–1939 (2018). https://doi.org/10.1038/s41559-018-0708-y

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