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Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation

Nature Plants volume 7, pages 481–499 (2021)Cite this article

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Abstract

Beneficial interactions between plant roots and rhizosphere microorganisms are pivotal for plant fitness. Nevertheless, the molecular mechanisms controlling the feedback between root architecture and microbial community structure remain elusive in maize. Here, we demonstrate that transcriptomic gradients along the longitudinal root axis associate with specific shifts in rhizosphere microbial diversity. Moreover, we have established that root-derived flavones predominantly promote the enrichment of bacteria of the taxa Oxalobacteraceae in the rhizosphere, which in turn promote maize growth and nitrogen acquisition. Genetic experiments demonstrate that LRT1-mediated lateral root development coordinates the interactions of the root system with flavone-dependent Oxalobacteraceae under nitrogen deprivation. In summary, these experiments reveal the genetic basis of the reciprocal interactions between root architecture and the composition and diversity of specific microbial taxa in the rhizosphere resulting in improved plant performance. These findings may open new avenues towards the breeding of high-yielding and nutrient-efficient crops by exploiting their interaction with beneficial soil microorganisms.

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Fig. 1: Interkingdom multiomics demonstrates causal plant–microbial interactions in the rhizosphere during root development.
Fig. 2: Host transcriptome and rhizosphere microbiome interactions affecting maize performance.
Fig. 3: Changes in rhizosphere microbiota conditioned by plant-derived flavones promote maize growth and nitrogen uptake in nitrogen-poor soil.
Fig. 4: Growth performance of mutants with lateral root defects is associated with flavone-conditioned rhizosphere microbiota.
Fig. 5: Flavonoid-dependent Oxalobacteraceae promote plant growth and nitrogen acquisition by triggering developmental feedback on lateral root formation in nitrogen-poor soil.
Fig. 6: Proposed model for flavone-dependent, microbiota-mediated lateral root formation and plant performance.

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Data availability

All raw plant RNA-seq data, rhizosphere bacterial 16S and fungal ITS and shotgun metagenomic sequencing data reported in this paper were deposited in the Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under accession no. SRP263360. RNA-seq reads were mapped to the maize reference genome sequence v.4 (https://www.maizegdb.org/genome/genome_assembly/Zm-B73-REFERENCE-GRAMENE-4.0). The SSUrRNA database from SILVA database (release 128, 2016, https://www.arb-silva.de/) and UNITE database (v.7.2, 2017, https://unite.ut.ee/) were used for analysis of bacterial 16S and fungal ITS sequences, respectively. The databases AgriGO (v.2.0, 2017, http://systemsbiology.cau.edu.cn/agriGOv2/) and REVIGO (2017, http://revigo.irb.hr/) were used for functional GO analysis of maize genes. Protein–protein interaction networks of enriched gene modules were generated by the database STRING (v.10.5, https://version-10-5.string-db.org/). Functional annotation of shotgun metagenomic sequencing was performed using COG databases (release clovr-1.0-RC9). We deposited customized scripts on the association of gene modules with microbial taxonomic traits in the following GitHub repository: https://github.com/PengYuMaize/Yu2021NaturePlants. Source data are provided with this paper.

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Acknowledgements

We thank P. Schulze-Lefert (Max Planck Institute for Plant Breeding Research, Cologne, Germany) for the generous donation of bacterial strains and natural soil for pot experiments. We thank J. Birchler (University of Missouri, Columbia, USA), C. Gardner (United States Department of Agriculture, Ames, USA), P. S. Schnable (Iowa State University, Ames, USA) and T. Wang (Chinese Academy of Agricultural Sciences, Beijing, China) for germplasm contribution. We thank S.-W. Lee (Dong-A University, Busan, Republic of Korea) and J. F. Kim (Yonsei University, Seoul, Republic of Korea) for sharing the methods used for rhizosphere transplantation. We thank C. Gutjahr (Technical University of Munich, Munich, Germany), C. Knief (University of Bonn, Bonn, Germany) and B. Niu (Northeast Forest University of China, Harbin, China) for valuable suggestions on the experiments. We thank the student helpers from C. Zou´s group at China Agricultural University (Beijing, China) for field sample harvesting. We thank A. Glogau (University of Bonn, Bonn, Germany) for nitrogen determination. This work is supported by Deutsche Forschungsgemeinschaft (DFG) grant nos. HO2249/9-3 and HO2249/12-1 (to F.H.) and YU272/1-1; Emmy Noether Programme (no. 444755415) to P.Y.; Germany’s Excellence Strategy (EXC 2070) PhenoRob grant no. 390732324 to G.S.; Bundesministerium für Bildung und Forschung grant no. 031B195C to F.H.; DFG Priority Program (SPP2089) ‘Rhizosphere Spatiotemporal Organisation – a Key to Rhizosphere Functions’ grant nos. 403671039 (to F.H. and P.Y.) and 403670038 (to B.S.R.). S.G.’s research is supported by Research Foundation – Flanders – Strategic Basic Research (grant no. 151553). K.T.’s research is supported by the Huazhong Agricultural University Scientific & Technological Self-innovation Foundation, the Max Planck Society and DFG grant no. SPP2125. X.C.’s research is supported by The Changjiang Scholarship, Ministry of Education, China, State Cultivation Base of Eco-agriculture for Southwest Mountainous Land (Southwest University, Chongqing, China) and the National Maize Production System in China (grant no. CARS-02-15).

Author information

Author notes

  1. These authors contributed equally: Peng Yu, Xiaoming He.

Authors and Affiliations

  1. College of Resources and Environment, and Academy of Agricultural Sciences, Southwest University, Chongqing, China

    Peng Yu, Xiaoming He, Xinping Chen & Frank Hochholdinger

  2. Crop Functional Genomics, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany

    Peng Yu, Xiaoming He, Marcel Baer, Felix P. Frey, Verena Bresgen & Frank Hochholdinger

  3. Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany

    Peng Yu, Xiaoming He & Verena Bresgen

  4. Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium

    Stien Beirinckx & Sofie Goormachtig

  5. Plant Sciences Unit, Flanders Research Institute for Agriculture Fisheries and Food, Merelbeke, Belgium

    Stien Beirinckx

  6. Center for Plant Systems Biology, VIB, Ghent, Belgium

    Stien Beirinckx & Sofie Goormachtig

  7. State Key Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing, China

    Tian Tian & Zhen Su

  8. Molecular Plant Nutrition, Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany

    Yudelsy A. T. Moya & Nicolaus von Wirén

  9. Department of Biogeochemistry of Agroecosystems, University of Göttingen, Göttingen, Germany

    Xuechen Zhang

  10. Plant Nutrition, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, Germany

    Marion Deichmann & Gabriel Schaaf

  11. Department of Plant Nutrition, College of Resources and Environmental Science, China Agricultural University, Beijing, China

    Chunjian Li

  12. Department of Soil and Plant Microbiome, Institute of Phytopathology, Christian-Albrecht University of Kiel, Kiel, Germany

    Bahar S. Razavi

  13. Botanical Institute, Cologne Biocenter, University of Cologne, Cologne, Germany

    Marcel Bucher

  14. Cluster of Excellence on Plant Sciences, University of Cologne, Cologne, Germany

    Marcel Bucher

  15. State Key Laboratory of Agricultural Microbiology, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, China

    Kenichi Tsuda

  16. Department of Plant Microbe Interactions, Max Planck Institute for Plant Breeding Research, Cologne, Germany

    Kenichi Tsuda

Authors
  1. Peng Yu
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  2. Xiaoming He
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  3. Marcel Baer
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  4. Stien Beirinckx
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  5. Tian Tian
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  6. Yudelsy A. T. Moya
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  7. Xuechen Zhang
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  8. Marion Deichmann
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  9. Felix P. Frey
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  10. Verena Bresgen
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  11. Chunjian Li
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  12. Bahar S. Razavi
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  13. Gabriel Schaaf
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  14. Nicolaus von Wirén
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  15. Zhen Su
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  16. Marcel Bucher
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  17. Kenichi Tsuda
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  18. Sofie Goormachtig
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  19. Xinping Chen
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  20. Frank Hochholdinger
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Contributions

P.Y., K.T., X.C. and F.H. designed the study. P.Y. and X.H. performed field and phytochamber experiments. P.Y., T.T., Z.S., F.P.F. and F.H. analysed transcriptome and microbiome data. P.Y. and V.B. performed shotgun metagenomic sequencing. Y.A.T.M. and N.v.W. performed targeted flavone profiling. X.Z. and B.S.R. performed 14C labelling and imaging analysis. M.D., G.S., Y.A.T.M. and N.v.W. conducted plant nutrient analysis. P.Y., X.H. and M. Baer performed bacterial inoculation experiments. S.B. and S.G. isolated Oxalobacteraceae strains from maize and performed in vivo analysis of bacterial strains and DR5::GUS in Arabidopsis. P.Y., X.H., S.B., B.S.R., G.S., N.v.W., M. Bucher, K.T., S.G., X.C. and F.H. wrote the paper. All authors read and approved the final version of the manuscript.

Corresponding authors

Correspondence to Xinping Chen or Frank Hochholdinger.

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The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Corné Pieterse, Klaus Schlaeppi and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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

Supplementary information

Supplementary Information

Supplementary Figs. 1–24 and Tables 1–4.

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Supplementary Data 1

Supplementary Datasets 1–15 (descriptions are shown individually in Excel sheets).

Supplementary Data 2

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Supplementary Data 7

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Supplementary Data 8

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Supplementary Data 9

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Supplementary Data 10

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Supplementary Data 11

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Source data

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Yu, P., He, X., Baer, M. et al. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nat. Plants 7, 481–499 (2021). https://doi.org/10.1038/s41477-021-00897-y

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