Abstract
Overyielding, the high productivity of multispecies plant communities, is commonly seen as the result of plant genetic diversity. Here we demonstrate that biodiversity–ecosystem functioning relationships can emerge in clonal plant populations through interaction with microorganisms. Using a model clonal plant species, we found that exposure to volatiles of certain microorganisms led to divergent plant phenotypes. Assembling communities out of plants associated with different microorganisms led to transgressive overyielding in both biomass and seed yield. Our results highlight the importance of belowground microbial diversity in plant biodiversity research and open new avenues for precision ecosystem management.
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Data availability
All data that support the findings of this study are available via Figshare at https://figshare.com/s/1094376bbb9259e1b18e.
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Acknowledgements
This study was supported by the National Natural Science Foundation of China (42350610257 (W.R.), 42377124 (W.R.), 42325704 (Z.W.), 42090064 (Q.S.), 42090062 (G.J.), 42007038 (G.J.) and 42277113 (Z.W.)), the Fundamental Research Funds for the Central Universities (XUEKEN2023044 (W.R.), KYT2023001 (Z.W.), KYCXJC2023007 (G.J.)), the Natural Science Foundation of Jiangsu Province (BK20230102 (G.J.)) the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant (838710-ReproDev (W.R.)), iDiv funded by the German Research Foundation (DFG–FZT 118, 202548816 (N.E.)) and the Jena Experiment funded by the DFG (FOR 5000). We thank R. Neher, R. Tschannen and S. Cretoiu for support with genome sequencing of bacterial strains used in this study.
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W.R., Z.W. and A.J. designed the experiments. W.R. carried out the experiments. W.R., G.J., Y.H. and A.J. analysed the data and wrote the manuscript. G.J., Z.W., G.A.K., Q.S. and N.E. revised the manuscript.
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Extended data
Extended Data Fig. 1 Experimental setup of the divided Petri plate for the exposure of clonal plants to bacterial volatiles.
Petri plate has two compartments divided by a wall, which provides physical separation of both compartments but allows the exchange of gases. In one compartment containing Murashige and Skoog agar medium, three seedlings of Arabidopsis were placed, while in the second compartment containing minimal salt agar medium, three 5 µl drops of bacterial culture were added at a distance of 3 cm from each other. Later, the plate was covered with a lid, sealed with parafilm and incubated for one week.
Extended Data Fig. 2 Comparison of genome sequences and volatile compounds produced by four bacterial strains.
(a) Genome to genome distance of four bacterial strains used for volatile compounds-mediated phenotypic induction of Arabidopsis thaliana Col-0. In the heatmap, higher intensity of red color represents higher genome-to-genome distance. (b) Principal component analysis (PCA) based on the relative peak area of volatile compounds produced by four bacterial strains in triplicate (n = 12). The volatile compounds analysis was conducted using gas chromatography-mass spectrometry (GC-MS). The four bacterial strains used in the study are Pseudoxanthomonas mexicana F12, Chryseobacterium daecheongense F23, Pseudoxanthomonas mexicana F31 and Pseudoxanthomonas sp. F37.
Extended Data Fig. 3 Effect of plant density on the four measured life-history traits (plant height, rosette area, aboveground biomass, number of siliques) with and without previous exposure to the volatile compounds produced by four different bacteria.
Plants were exposed to the volatile compounds of four different bacteria during early life for one-week (representing four different phenotypes); later, bacteria were removed, and plants were placed together in pots at 1-, 2-, and 4-plants density (PD) and 1-, 2-, and 4-plants phenotypic diversity (HD) levels, respectively. In scatterplot panels, each data point represents the mean value of quadruplicates (n = 28). The colors of data points and regression lines correspond to the plant phenotypic diversity levels.
Extended Data Fig. 4 Development of plant height and rosette area after 10 days, 25 days and 35 days with and without previous exposure to the volatile compounds of four different bacteria.
Plants were exposed to volatile compounds of four different bacteria during early life for one-week (representing four different phenotypes); later, bacteria were removed, and plants were placed together in pots at 1-, 2- and 4-plants density and 1- 2- and 4-plants phenotypic diversity levels, respectively. In scatterplot panels, each data point represents the mean value of quadruplicates (n = 28). The colors of data points and regression lines correspond to the plant phenotypic diversity levels.
Extended Data Fig. 5 Pairwise interactions between plant phenotypes for the four-plant life-history traits (plant height, rosette area, aboveground biomass, number of siliques).
Pairwise interactions between plant phenotypes were determined as the relative interaction index (RII) separately at 2- and 4-plants density levels using only a diversity level of 2-phenotypes for each of the four life-history traits. Pairwise RII was defined as the performance of each phenotype in the presence of another phenotype, relative to its performance in monoculture at the same plant density. Red arrows stand for competition and green arrows stand for facilitation. Arrow breadth is proportional to |RII|. Only arrows showing significant differences according to the two-tailed T-test at P < 0.05 are included.
Extended Data Fig. 6 Sampling effect of plant phenotypes on life-history traits (plant height, rosette area, aboveground biomass, number of siliques).
Sampling effect was determined at the highest tested density of four plants per pot, covering diversity levels of 2- and 4-phenotypes. It was calculated by carrying out two-tailed T-test comparing the performance of communities containing the phenotype relative to those lacking it. In the heatmap, the higher intensity of green color represents a significant sampling effect while the higher intensity of red color represents a nonsignificant sampling effect based on P values provided. The four bacterial strains used to induce plant phenotypes are Pseudoxanthomonas mexicana F12, Chryseobacterium daecheongense F23, Pseudoxanthomonas mexicana F31 and Pseudoxanthomonas sp. F37.
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Supplementary Text and Tables 1–4.
Supplementary Data
Supplementary Data 1. Volatile compounds-mediated plant growth promoting potential of bacterial strains isolated from the tomato rhizosphere at the flowering stage. Supplementary Data 2. Identification of volatile compounds produced by four bacterial strains used for volatile compounds-mediated phenotypic induction of Arabidopsis thaliana Col-0.
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Raza, W., Jiang, G., Eisenhauer, N. et al. Microbe-induced phenotypic variation leads to overyielding in clonal plant populations. Nat Ecol Evol 8, 392–399 (2024). https://doi.org/10.1038/s41559-023-02297-1
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DOI: https://doi.org/10.1038/s41559-023-02297-1
