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.

  • Article
  • Published:

Root microbiota confers rice resistance to aluminium toxicity and phosphorus deficiency in acidic soils

Abstract

Aluminium (Al) toxicity impedes crop growth in acidic soils and is considered the second largest abiotic stress after drought for crops worldwide. Despite remarkable progress in understanding Al resistance in plants, it is still unknown whether and how the soil microbiota confers Al resistance to crops. Here we found that a synthetic community composed of highly Al-resistant bacterial strains isolated from the rice rhizosphere increased rice yield by 26.36% in acidic fields. The synthetic community harvested rhizodeposited carbon for successful proliferation and mitigated soil acidification and Al toxicity through extracellular protonation. The functional coordination between plants and microbes offers a promising way to increase the usage of legacy phosphorus in topsoil. These findings highlight the potential of microbial tools for advancing sustainable agriculture in acidic soils.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: SynCom promotes rice performance under Al-toxic acidic stress.
Fig. 2: Effects of SynCom inoculation on rice root architecture under different treatment conditions.
Fig. 3: Variation in soil chemical properties and bacterial communities after SynCom inoculation.
Fig. 4: The colonization of SynCom assists rice in obtaining surface soil phosphorous under Al-toxic acidic stress.
Fig. 5: Enhanced Al-resistant response in rice provides more carbon for the root microbiota.
Fig. 6: A schematic model summarizing the hypothesized mechanisms of how SynCom confers rice Al resistance and plant growth in acidic soil.

Similar content being viewed by others

Data availability

The raw sequence data reported in this paper have been deposited (PRJCA011216) in the Genome Sequence Archive in the BIG Data Center62, Chinese Academy of Sciences under accession code CRA007891 for Rhodococcus erythropolis transcriptome sequencing, CRA007889 for Pseudomonas aeruginosa transcriptome sequencing, CRA008623 for bacterial 16S rRNA gene sequencing data in the 13C isotope labelling experiment, CRA007869 for phoD gene sequencing, CAR007871 for rice leaf transcriptome sequencing, and CAR008056 for rice root transcriptome sequencing in the pot experiment and are publicly accessible at http://bigd.big.ac.cn/gsa. All pure strains were deposited in the CNGB Sequence Archive (CNSA)63 of the China National GeneBank DataBase (CNGBdb)64 at https://db.cngb.org/ with accession number CNP0003393. Source data are provided with this paper.

Code availability

The code used for this work is available from the corresponding author on request.

References

  1. Kochian, L. V., Piñeros, M. A., Liu, J. & Magalhaes, J. V. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu. Rev. Plant Biol. 66, 571–598 (2015).

    Article  CAS  PubMed  Google Scholar 

  2. von Uexküll, H. R. & Mutert, E. Global extent, development and economic impact of acid soils. Plant Soil 171, 1–15 (1995).

    Article  Google Scholar 

  3. Yang, Z., Rao, I. M. & Horst, W. J. Interaction of aluminium and drought stress on root growth and crop yield on acid soils. Plant Soil 372, 3–25 (2013).

    Article  CAS  Google Scholar 

  4. Kochian, L. V., Hoekenga, O. A. & Piñeros, M. A. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu. Rev. Plant Biol. 55, 459–493 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Siqueira, J. A., Silva, M. F., Wakin, T., Nunes-Nesi, A. & Araujo, W. L. Metabolic and DNA checkpoints for the enhancement of Al tolerance. J. Hazard. Mater. 430, 128366 (2022).

    Article  CAS  PubMed  Google Scholar 

  6. Chandra, J. & Keshavkant, S. Mechanisms underlying the phytotoxicity and genotoxicity of aluminum and their alleviation strategies: a review. Chemosphere 278, 130384 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  7. Magalhaes, J. V., Piñeros, M. A., Maciel, L. S. & Kochian, L. V. Emerging pleiotropic mechanisms underlying aluminum resistance and phosphorus acquisition on acidic soils. Front. Plant Sci. 9, 1420 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kochian, L. V., Pineros, M. A. & Hoekenga, O. A. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274, 175–195 (2005).

    Article  CAS  Google Scholar 

  9. Delhaize, E., Ma, J. F. & Ryan, P. R. Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci. 17, 341–348 (2012).

    Article  CAS  PubMed  Google Scholar 

  10. Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020).

    Article  CAS  PubMed  Google Scholar 

  11. Nerva, L. et al. Breeding toward improved ecological plant-microbiome interactions. Trends Plant Sci. 27, 1134–1143 (2022).

    Article  CAS  PubMed  Google Scholar 

  12. Durán, P. et al. Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175, 973–983 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Narayanan, M. & Ma, Y. Metal tolerance mechanisms in plants and microbe-mediated bioremediation. Environ. Res. 222, 115413 (2023).

    Article  CAS  PubMed  Google Scholar 

  14. Rajkumar, M., Sandhya, S., Prasad, M. N. & Freitas, H. Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 30, 1562–1574 (2012).

    Article  CAS  PubMed  Google Scholar 

  15. Vorholt, J. A., Vogel, C., Carlström, C. I. & Müller, D. B. Establishing causality: opportunities of synthetic communities for plant microbiome research. Cell Host Microbe 22, 142–155 (2017).

    Article  CAS  PubMed  Google Scholar 

  16. Zhang, J. et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37, 676–684 (2019).

    Article  CAS  PubMed  Google Scholar 

  17. Carlström, C. I. et al. Synthetic microbiota reveal priority effects and keystone strains in the Arabidopsis phyllosphere. Nat. Ecol. Evol. 3, 1445–1454 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Carrión, V. J. et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366, 606–612 (2019).

    Article  ADS  PubMed  Google Scholar 

  19. Schmitz, L. et al. Synthetic bacterial community derived from a desert rhizosphere confers salt stress resilience to tomato in the presence of a soil microbiome. ISME J. 16, 1907–1920 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sukweenadhi, J. et al. Paenibacillus yonginensis DCY84T induces changes in Arabidopsis thaliana gene expression against aluminum, drought, and salt stress. Microbiol. Res. 172, 7–15 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Silambarasan, S., Logeswari, P., Cornejo, P., Abraham, J. & Valentine, A. Simultaneous mitigation of aluminum, salinity and drought stress in Lactuca sativa growth via formulated plant growth promoting Rhodotorula mucilaginosa CAM4. Ecotox. Environ. Saf. 180, 63–72 (2019).

    Article  CAS  Google Scholar 

  22. Gooderham, W. J. & Hancock, R. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 33, 279–294 (2009).

    Article  CAS  PubMed  Google Scholar 

  23. de Carvalho, C. C. C. R. & Da Fonseca, M. M. R. The remarkable Rhodococcus erythropolis. Appl. Microbiol. Biot. 67, 715–726 (2005).

    Article  Google Scholar 

  24. Goulding, K. W. T. & Blake, L. Land use, liming and the mobilization of potentially toxic metals. Agr. Ecosyst. Environ. 67, 135–144 (1998).

    Article  CAS  Google Scholar 

  25. Huang, G. et al. Rice actin binding protein RMD controls crown root angle in response to external phosphate. Nat. Commun. 9, 2346 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  26. Lidbury, I. D. E. A. et al. A widely distributed phosphate-insensitive phosphatase presents a route for rapid organophosphorus remineralization in the biosphere. Proc. Natl Acad. Sci. USA 119, e2118122119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nkoh, J. N., Yan, J., Xu, R., Shi, R. & Hong, Z. The mechanism for inhibiting acidification of variable charge soils by adhered Pseudomonas fluorescens. Environ. Pollut. 260, 114049 (2020).

    Article  CAS  PubMed  Google Scholar 

  28. Nannipieri, P., Giagnoni, L., Landi, L. & Renella, G. Phosphorus in Action. Soil Biology Vol. 26 (Springer, 2010).

  29. Zimmerman, A. E., Martiny, A. C. & Allison, S. D. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J. 7, 1187–1199 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Moudrikova, S. et al. Quantification of polyphosphate in microalgae by Raman microscopy and by a reference enzymatic assay. Anal. Chem. 89, 12006–12013 (2017).

    Article  CAS  PubMed  Google Scholar 

  31. Yoshida, N. et al. A unique intracellular compartment formed during the oligotrophic growth of Rhodococcus erythropolis N9T-4. Appl. Microbiol. Biot. 101, 331–340 (2017).

    Article  CAS  Google Scholar 

  32. Zhong, C., Fu, J., Jiang, T., Zhang, C. & Cao, G. Polyphosphate metabolic gene expression analyses reveal mechanisms of phosphorus accumulation and release in Microlunatus phosphovorus strain JN459. FEMS Microbiol. Lett. 365, fny034 (2018).

  33. Paszkowski, U., Kroken, S., Roux, C. & Briggs, S. P. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl Acad. Sci. USA 99, 13324–13329 (2002).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  34. Li, J. et al. Natural variation underlies alterations in Nramp aluminum transporter (NRAT1) expression and function that play a key role in rice aluminum tolerance. Proc. Natl Acad. Sci. USA 111, 6503–6508 (2014).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vives-Peris, V., de Ollas, C., Gómez-Cadenas, A. & Pérez-Clemente, R. M. Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep. 39, 3–17 (2019).

    Article  PubMed  Google Scholar 

  36. Li, H. et al. Active antibiotic resistome in soils unraveled by single-cell isotope probing and targeted metagenomics. Proc. Natl Acad. Sci. USA 119, e2093494177 (2022).

    Article  Google Scholar 

  37. Frąc, M., Hannula, S. E., Bełka, M. & Jęyczka, M. Fungal biodiversity and their role in soil health. Front. Microbiol. 9, 707 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Chen, Q. et al. Potential of indigenous crop microbiomes for sustainable agriculture. Nat. Food 2, 233–240 (2021).

  39. Hartmann, M. & Six, J. Soil structure and microbiome functions in agroecosystems. Nat. Rev. Earth Env. 4, 4–18 (2023).

    Article  Google Scholar 

  40. Saad, M. M., Eida, A. A., Hirt, H. & Doerner, P. Tailoring plant-associated microbial inoculants in agriculture: a roadmap for successful application. J. Exp. Bot. 71, 3878–3901 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Singh, B. K., Trivedi, P., Egidi, E., Macdonald, C. A. & Delgado-Baquerizo, M. Crop microbiome and sustainable agriculture. Nat. Rev. Microbiol. 18, 601–602 (2020).

    Article  CAS  PubMed  Google Scholar 

  42. Shaheen, S. M., Hooda, P. S. & Tsadilas, C. D. Opportunities and challenges in the use of coal fly ash for soil improvements—a review. J. Environ. Manage. 145, 249–267 (2014).

    Article  CAS  PubMed  Google Scholar 

  43. Hammerschmitt, R. K. et al. Limestone and gypsum reapplication in an oxisol under no-tillage promotes low soybean and corn yield increase under tropical conditions. Soil Till. Res. 214, 105165 (2021).

    Article  Google Scholar 

  44. Gascho, G. J. & Parker, M. B. Long-term liming effects on coastal plain soils and crops. Agron. J. 93, 1305–1315 (2001).

    Article  Google Scholar 

  45. Sridhar, B. et al. Microbial community shifts correspond with suppression of decomposition 25 years after liming of acidic forest soils. Global Change Biol. 28, 5399–5415 (2022).

    Article  CAS  Google Scholar 

  46. Zhuang, X., Chen, J., Shim, H. & Bai, Z. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ. Int. 33, 406–413 (2007).

    Article  PubMed  Google Scholar 

  47. Cordell, D. & White, S. Life’s bottleneck: sustaining the world’s phosphorus for a food secure future. Annu. Rev. Env. Resour. 39, 161–188 (2014).

    Article  Google Scholar 

  48. Zou, T., Zhang, X. & Davidson, E. A. Global trends of cropland phosphorus use and sustainability challenges. Nature 611, 81–87 (2022).

    Article  ADS  CAS  PubMed  Google Scholar 

  49. Kinraide, T. B. A. S. Identity of the rhizotoxic aluminium species. Plant Soil 134, 167–178 (1991).

    Article  CAS  Google Scholar 

  50. Famoso, A. N. et al. Development of a novel aluminum tolerance phenotyping platform used for comparisons of cereal aluminum tolerance and investigations into rice aluminum tolerance mechanisms. Plant Physiol. 153, 1678–1691 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Shaff, J. E., Schultz, B. A., Craft, E. J., Clark, R. T. & Kochian, L. V. GEOCHEM-EZ: a chemical speciation program with greater power and flexibility. Plant Soil 330, 207–214 (2010).

    Article  CAS  Google Scholar 

  52. Tiessen, H. & Moir, J. O. Soil Sampling and Methods of Analysis Ch. 25 (Lewis Publishers, 1993).

  53. Parada, A. E., Needham, D. M. & Fuhrman, J. A. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ. Microbiol. 18, 1403–1414 (2016).

    Article  CAS  PubMed  Google Scholar 

  54. Fish, J. A. et al. FunGene: the functional gene pipeline and repository. Front. Microbiol. 4, 291 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Sakurai, M., Wasaki, J., Tomizawa, Y., Shinano, T. & Osaki, M. Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci. Plant Nutr. 54, 62–71 (2008).

    Article  CAS  Google Scholar 

  56. Luo, G. et al. Understanding how long-term organic amendments increase soil phosphatase activities: Insight into phoD- and phoC-harboring functional microbial populations. Soil Biol. Biochem. 139, 107632 (2019).

    Article  CAS  Google Scholar 

  57. Eichorst, S. A. et al. Advancements in the application of NanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils. FEMS Microbiol. Ecol. 91, fiv106 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Li, H. et al. D2O-isotope-labeling approach to probing phosphate-solubilizing bacteria in complex soil communities by single-cell Raman spectroscopy. Anal. Chem. 91, 2239–2246 (2019).

    Article  CAS  PubMed  Google Scholar 

  59. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. RSEM (RNA-seq by expectation-maximization). GitHub https://deweylab.github.io/RSEM (2018).

  62. BIG, D. C. M. Database resources of the BIG Data Center in 2018. Nucleic Acids Res. 46, D14–D20 (2018).

    Article  Google Scholar 

  63. Guo, X. et al. CNSA: a data repository for archiving omics data. Database 2020, baaa055 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  64. Chen, F. et al. CNGBdb: China National GeneBank DataBase. Hereditas 42, 799–809 (2020).

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. E. Shaff and E. J. Craft (Robert W. Holley Center of Agriculture and health, USDA-ARS, Cornell University) for providing the helpful tool Geochem-EZ software. We thank C. Huang (Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences) and G. Huang (School of Life Sciences and Biotechnology, Shanghai Jiao Tong University) for critical discussion and feedback on the paper. We thank J. Fan, M. Liu, X. Liu and L. Chen from the Yingtan Agroecosystem Field Experiment Station of the Chinese Academy of Sciences for field experiment management and sampling assistance. We received fundings from Strategic Priority Research Program of the Chinese Academy of Sciences (XDA24020104 to Y.L.), National Key R&D Program of China (2021YFD1900400 to Y.L.), National Natural Science Foundation of China (42377121 to Y.L.), Innovation Program of Institute of Soil Science (ISSASIP2201 to Y.L.) and Youth Innovation Promotion Association of Chinese Academy of Sciences (2016284 to Y.L.). The funders had roles in study design and data collection and analysis.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: Y.L., Y.B., T.W.C., R.S. and J. Zhang. Methodology: Y.L., C.L., M.J., M.M.Y., Z.M., Y.B., L.Z., Y.W., J.D., W.L. and J. Zhou. Investigation: Y.L., C.L., M.J. and M.M.Y. Data curation: C.L., M.J., M.M.Y., Z.M., L.Z. and J.D. Formal analysis: Y.L., C.L., M.J., M.M.Y., Z.M. and L.Z. Supervision: Y.L., E.W., R.S. and J. Zhang. Writing—original draft: Y.L., C.L., M.J. and M.M.Y. Writing—review and editing: C.L., M.J., M.M.Y., Y.L., E.W., Y.B., T.W.C., J. Zhou, Z.M., L.Z., Y.W., J.D., W.L., B.S., R.S. and J. Zhang.

Corresponding author

Correspondence to Yuting Liang.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Food thanks Hongwei Liu, Miguel Pineros and Qing Yao for their contribution to the peer review of this work.

Additional information

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–25, text and methods.

Reporting Summary

Supplementary Table

Supplementary Table 1. Strain information. Supplementary Table 2. Parameters of the logistic models of Rhodococcus erythropolis and Pseudomonas aeruginosa growing under different Al3+ conditions. Supplementary Table 3. Intensity of differential metabolites in rice roots with and without SynCom. Supplementary Table 4. Ionic interactions predicted by Geochem-EZ. Supplementary Table 5. Physicochemical properties of experimental soils collected from the field.

Supplementary Data

Source data of Supplementary Figs. 2–10, 12–14, 16, 19–23 and 25.

Supplementary Video 1

3D video of rice root under Al3+ stress.

Supplementary Video 2

3D video of rice root under Al3+ stress with SynCom inoculation.

Supplementary Video 3

3D video of rice root under limed condition.

Supplementary Video 4

3D video of rice root under limed condition with SynCom inoculation.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Jiang, M., Yuan, M.M. et al. Root microbiota confers rice resistance to aluminium toxicity and phosphorus deficiency in acidic soils. Nat Food 4, 912–924 (2023). https://doi.org/10.1038/s43016-023-00848-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s43016-023-00848-0

This article is cited by

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