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

Authors: YU, PENG - University Of Bonn; LI, CHUNHUI - Chinese Academy Of Agricultural Sciences; LI, MENG - Pennsylvania State University; HE, XIAOMING - University Of Bonn; WANG, DANNING - University Of Bonn; LI, HONGJIE - University Of Bonn; MARCON, CAROLINE - University Of Bonn; TEGETHOF, HENDRIK - University Of Bonn; PEREZ-LIMÓN, SERGIO - Pennsylvania State University; CHEN, XINPING - Southwest University; DELGADO-BAQUERIZO, MANUEL - Instituto De Recursos Naturales Y Agrobiologia De Sevilla (IRNAS-CSIC); KOLLER, ROBERT - Forschungszentrum Juelich Gmbh; METZNER, RALF - Forschungszentrum Juelich Gmbh; VAN DUSSCHOTEN, DAGMAR - Forschungszentrum Juelich Gmbh; BORISJUK, LJUDMILLA - Leibniz Institute Of Plant Genetics And Crop Plant Research; PLUTENKO, IAROSLAV - Leibniz Institute Of Plant Genetics And Crop Plant Research; RESENDE, MARIO - University Of Florida; Bernau, Vivian; SALVI, SILVIO - University Of Bologna; AKALE, ASEGIDEW - University Of Bayreuth; ABDALLA, MOHANNED - University Of Bayreuth; AHMED, MUTEZ ALI - University Of Bayreuth; BAUER, FELIX - Forschungszentrum Juelich Gmbh; SCHNEPF, ANDREA - Forschungszentrum Juelich Gmbh; LOBET, GUILLAUME - Forschungszentrum Juelich Gmbh; HEYMANS, ADRIEN - Universite Catholique; SURESH, KIRAN - University Of Bonn; SCHREIBER, LUKAS - University Of Bonn; MCLAUGHLIN, CHLOEE - University Of Bonn; LI, CHUNJIAN - China Agricultural University; SAWERS, RUAIRIDH - Pennsylvania State University; WANG, TIANYU - Chinese Academy Of Agricultural Sciences; HOCHHOLDINGER, FRANK - University Of Bonn

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/19/2024
Publication Date: 5/22/2024
Citation: Yu, P., Li, C., Li, M., He, X., Wang, D., Li, H., Marcon, C., Tegethof, H., Perez-Limón, S., Chen, X., Delgado-Baquerizo, M., Koller, R., Metzner, R., Van Dusschoten, D., Borisjuk, L., Plutenko, I., Resende, M.R., Bernau, V.M., Salvi, S., Akale, A., Abdalla, M., Ahmed, M., Bauer, F.M., Schnepf, A., Lobet, G., Heymans, A., Suresh, K., Schreiber, L., Mclaughlin, C.M., Li, C., Sawers, R.J., Wang, T., Hochholdinger, F. 2024. Seedling root system adaptation to water availability during maize domestication and global expansion. Nature Genetics. 56:1245-1256. https://doi.org/10.1038/s41588-024-01761-3.
DOI: https://doi.org/10.1038/s41588-024-01761-3

Interpretive Summary: Crops form complex root systems that forage for soil resources and are key to productivity. It has been proposed that, during domestication, root systems have been the targets of indirect selection, playing a role in crop adaptation to new agricultural environments. Yet, to date, it is unknown what this adaptation of root traits to their novel local habitats occurred. In this study we explore variation in seminal root number in maize. We characterised >9,000 accessions of wild and cultivated corn, sampling the global spectrum of cultivated varieties and maize wild-relatives. We demonstrate that seminal root production greatly increased during maize domestication and that variation in seminal root number within cultivated maize is correlated with the local environment. While tropical maize typically produces 5 to 10 seminal roots, the number fell in temperate varieties. Candidate genes linked to both environmental variation and seminal root number were identified. One gene was functionally characterized and modelling supported an adaptive advantage of reducing seminal root number under drought conditions to drive a reshaping of seedling root architecture.

Technical Abstract: Crops form complex three-dimensional root systems that forage for soil resources and are key to productivity. It has been proposed that during domestication root systems have been the targets of indirect selection, playing a role in crop adaptation to new agricultural environments. Yet, to date, it is unknown what this adaptation of root traits to their novel local habitats occurred. In this study, we define the ecological signatures and genomic basis of variation in seminal root number in maize. We characterised >9,000 accessions across the genus Zea sampling the global spectrum of cultivated varieties and maize wild-relatives. We demonstrate that seminal root production greatly increased during maize domestication and that variation in seminal root number within cultivated maize is correlated with the local environment. While tropical maize typically produces 5 to 10 seminal roots, the number fell in temperate varieties, the Northern Flints producing few if any seminal roots, in line with values seen in maize wild relatives. Environmental and phenotypic association analyses, and linkage mapping identified candidate genes linked to both environmental variation and seminal root number. Functional characterization of the candidate gene ZmHb77 and in silico root modelling supported an adaptive advantage of reducing seminal root number under drought conditions to drive a reshaping of seedling root architecture.