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Seedling root system adaptation to water availability during maize domestication and global expansion

Nature Genetics volume 56, pages 1245–1256 (2024)Cite this article

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Abstract

The maize root system has been reshaped by indirect selection during global adaptation to new agricultural environments. In this study, we characterized the root systems of more than 9,000 global maize accessions and its wild relatives, defining the geographical signature and genomic basis of variation in seminal root number. We demonstrate that seminal root number has increased during maize domestication followed by a decrease in response to limited water availability in locally adapted varieties. By combining environmental and phenotypic association analyses with linkage mapping, we identified genes linking environmental variation and seminal root number. Functional characterization of the transcription factor ZmHb77 and in silico root modeling provides evidence that reshaping root system architecture by reducing the number of seminal roots and promoting lateral root density is beneficial for the resilience of maize seedlings to drought.

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Fig. 1: Maize evolutionary history resolves global organization of SRN.
Fig. 2: Geographical and genomic signatures of SRN variation in Mexico.
Fig. 3: Variation in SRN coincides with proportional origin from Northern Flint maize sources.
Fig. 4: Variation in SRN drives overall root architectural and hydraulic properties.
Fig. 5: Functional characterization of ZmHb77 controlling root traits and drought tolerance.
Fig. 6: Natural variation of the ZmHb77 allele and its contribution to root architecture and drought tolerance in maize seedlings.

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Data availability

All raw seminal root phenotyping data, geographical coordinates and soil modeling data are provided in Supplementary Tables 1–8. All germplasm information that is the geographically diverse teosinte accessions, maize traditional varieties and inbred lines contributed by NCRPIS, CIMMYT and the Chinese maize seed germplasm bank at the Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (China) used in this study are summarized in the Supplementary Tables 1–5. Geographical coordinates and elevation information of the collection sites for the traditional maize varieties were retrieved from the public database of the US National Plant Germplasm System (https://www.grin-global.org). Soil and climate data were collected from WorldClim (https://worldclim.org), the NCEP/NCAR Reanalysis Project (https://psl.noaa.gov/data/reanalysis/reanalysis.shtml), NASA SRB (https://asdc.larc.nasa.gov/project/SRB), Climate Research Unit (https://www.uea.ac.uk/groups-and-centres/climatic-research-unit), SoilGrids (https://soilgrids.org v.2) and the Global Soil Dataset (https://www.fao.org/soils-portal/data-hub/soil-maps-and-databases/harmonized-world-soil-database-v12/en). Maize genome resequencing data of the Gaspé Flint introgression panel and root RNA sequencing data were deposited in the Sequence Read Archive (http://www.ncbi.nlm.nih.gov/sra) under the BioProject ID PRJNA1095206. Source data are provided with this paper.

Code availability

The customized scripts included in this study are available at GitHub (https://github.com/PengYuMaize/GlobalSeminalRoot) with https://doi.org/10.5281/zenodo.10985812 (ref. 83).

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Acknowledgements

We thank J. Ross-Ibarra (University of California–Davis, USA) for comments on the manuscript. We are grateful to the North Central Regional Plant Introduction Station (NCRPIS, USDA-ARS and Iowa State University, Ames, Iowa, USA) and the International Maize and Wheat Improvement Center (CIMMYT) for providing seeds for this work. NCRPIS is part of the USDA-ARS National Plant Germplasm System. We thank A. Charcosset (GQE‐Le Moulon, INRAE, Univ. Paris‐Sud, CNRS, AgroParisTech, Université Paris‐Saclay, Gif‐sur‐Yvette, France) and M. López Luaces (Centro Investigacións Agrarias Mabegondo, Spain) for contributing European maize germplasm. We thank S. Mayer and S. Wagner (Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany) for technical support for NMR, and S. Ortleb, L. Kalms and P. Hinrichs (Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany) for image segmentation. We thank S. Siemens, A. Brox and H. Rehkopf (Crop Functional Genomics, INRES, University of Bonn, Germany) for root phenotyping and DNA extraction. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) grants HO2249/22-1 to F.H. and YU272/1-1 to P.Y., the DFG Emmy Noether Programme (444755415 to P.Y.), the DFG SPP2089 “Rhizosphere spatiotemporal organisation—a key to rhizosphere functions” (403671039 to F.H. and P.Y., 403641034 to A.S.), the USDA National Institute of Food and Agriculture and Hatch Appropriations (PEN04734 and 1021929 to R.J.H.S.), Consejo Nacional de Ciencia Tecnologia (FOINS-2016-01 to R.J.H.S.), National Science Foundation (1546719 to R.J.H.S.), the National Key Research and Development Program of China (2021YFD1200700, 2016 YFD0100103 and 2020YFE0202300 to T.W.), the Innovation Program of Chinese Academy of Agricultural Sciences to T.W., the Innovation Research 2035 Pilot Plan of Southwest University (SWU-XDZD22001 to X.C.), the US Department of Agriculture, Agricultural Research Service (USDA-ARS) to V.B., the TED2021-130908B-C41/AEI/10.13039/501100011033/Unión Europea NextGenerationEU/PRTR and the Spanish Ministry of Science and Innovation for the I + D + i project PID2020-115813RA-I00 funded by MCIN/AEI/10.13039/501100011033 to M.D. This work was partially funded by the DFG under Germany’s Excellence Strategy–EXC 2070 (390732324 to P.Y. and A.S.). R.K., D.v.D., R.M. and D.P. acknowledge support from the Helmholtz Association for the Forschungszentrum Jülich GmbH and thank A. Chlubek, G. Huber and J. Bühler for technical support with MRI and PET. The germplasm propagation is funded by the TRA Sustainable Futures (University of Bonn) as part of the Excellence Strategy of the federal and state governments.

Author information

Author notes

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

Authors and Affiliations

  1. Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany

    Peng Yu, Xiaoming He, Danning Wang, Hongjie Li, Caroline Marcon & Frank Hochholdinger

  2. Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany

    Peng Yu, Xiaoming He, Danning Wang & Hongjie Li

  3. State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, PR China

    Chunhui Li, Yu Li & Tianyu Wang

  4. Department of Plant Science, The Pennsylvania State University, State College, PA, USA

    Meng Li, Sergio Perez-Limón & Ruairidh J. H. Sawers

  5. College of Resources and Environment, and Academy of Agricultural Sciences, Southwest University (SWU), Chongqing, PR China

    Xinping Chen

  6. Laboratorio de Biodiversidad y Funcionamiento Ecosistémico. Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain

    Manuel Delgado-Baquerizo

  7. Unidad Asociada CSIC-UPO (BioFun), Universidad Pablo de Olavide, Sevilla, Spain

    Manuel Delgado-Baquerizo

  8. Institute of Bio- and Geosciences, Plant Sciences (IBG-2), Forschungszentrum Juelich GmbH, Juelich, Germany

    Robert Koller, Ralf Metzner, Dagmar van Dusschoten & Daniel Pflugfelder

  9. Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany

    Ljudmilla Borisjuk & Iaroslav Plutenko

  10. Horticultural Sciences Department, University of Florida, Gainesville, FL, USA

    Audrey Mahon & Marcio F. R. Resende Jr.

  11. Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy

    Silvio Salvi

  12. Chair of Root-Soil Interactions, TUM School of Life Sciences, Technical University of Munich, Freising, Germany

    Asegidew Akale, Mohanned Abdalla & Mutez Ali Ahmed

  13. Institute of Bio- and Geosciences, Agrosphere (IBG-3), Forschungszentrum Jülich GmbH, Jülich, Germany

    Felix Maximilian Bauer, Andrea Schnepf & Guillaume Lobet

  14. Earth and Life Institute, Université catholique de Louvain, UCLouvain, Belgium

    Guillaume Lobet & Adrien Heymans

  15. Institute of Cellular and Molecular Botany (IZMB), Department of Ecophysiology, University of Bonn, Bonn, Germany

    Kiran Suresh & Lukas Schreiber

  16. Intercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, State College, PA, USA

    Chloee M. McLaughlin

  17. Key Laboratory of Plant-Soil Interactions, College of Resources and Environmental Sciences, National Academy of Agriculture Green Development, Ministry of Education, China Agricultural University, Beijing, PR China

    Chunjian Li

  18. Plant Breeding, TUM School of Life Sciences, Technical University of Munich, Freising, Germany

    Manfred Mayer & Chris-Carolin Schön

  19. North Central Regional Plant Introduction Station, USDA-Agriculture Research Service and Iowa State University, Ames, IA, USA

    Vivian Bernau

  20. Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany

    Nicolaus von Wirén

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  1. Peng Yu
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Contributions

P.Y. and F.H. conceived and designed the project. P.Y. coordinated the project. P.Y., C.-H.L., X.H., H.L., A.M., M.F.R.R.J., M.M., C.-C.S. and C.M. performed phenotyping, collected and prepared samples. P.Y., C.-H.L., M.L., D.W., R.J.H.S., T.W. and F.H. conducted bioinformatics analyses and analyzed data. R.K., R.M., D.v.D. and D.P. performed MRI–PET root imaging and analyzed data. L.B. and I.P. performed NMR seed imaging and analyzed data. M.L., S.P., C.M.M., M.D. and R.J.H.S. performed ecological and environmental analyses. F.M.B., A.S., G.L. and A.H. performed structural–functional modeling analyses. A.A., M.A. and M.A.A. performed the soil hydraulic modeling experiment and data analyses. K.S. and L.S. performed lignin analyses. Y.L., X.C., S.S., V.B., N.v.W., C.-J.L. and T.W. contributed valuable suggestions for the analysis and interpretation of results. P.Y., C.-H.L., M.L., R.J.H.S., T.W. and F.H. wrote the manuscript. All authors read and approved the paper.

Corresponding authors

Correspondence to Peng Yu, Ruairidh J. H. Sawers, Tianyu Wang or Frank Hochholdinger.

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Yu, P., Li, C., Li, M. et al. Seedling root system adaptation to water availability during maize domestication and global expansion. Nat Genet 56, 1245–1256 (2024). https://doi.org/10.1038/s41588-024-01761-3

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