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

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 18. 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 15. 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.

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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.

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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 (2024). https://doi.org/10.1038/s41588-024-01761-3

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