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

Peng Yu^#^{1

2}, Chunhui Li^#³, Meng Li^#⁴, Xiaoming He^#^{5

6}, Danning Wang^{5

6}, Hongjie Li^{5

6}, Caroline Marcon⁵, Yu Li³, Sergio Perez-Limón⁴, Xinping Chen⁷, Manuel Delgado-Baquerizo^{8

9}, Robert Koller¹⁰, Ralf Metzner¹⁰, Dagmar van Dusschoten¹⁰, Daniel Pflugfelder¹⁰, Ljudmilla Borisjuk¹¹, Iaroslav Plutenko¹¹, Audrey Mahon¹², Marcio F R Resende Jr¹², Silvio Salvi¹³, Asegidew Akale¹⁴, Mohanned Abdalla¹⁴, Mutez Ali Ahmed¹⁴, Felix Maximilian Bauer¹⁵, Andrea Schnepf¹⁵, Guillaume Lobet^{15

16}, Adrien Heymans¹⁶, Kiran Suresh¹⁷, Lukas Schreiber¹⁷, Chloee M McLaughlin¹⁸, Chunjian Li¹⁹, Manfred Mayer²⁰, Chris-Carolin Schön²⁰, Vivian Bernau²¹, Nicolaus von Wirén²², Ruairidh J H Sawers²³, Tianyu Wang²⁴, Frank Hochholdinger²⁵

Affiliations

¹ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. yupeng@uni-bonn.de.
² Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. yupeng@uni-bonn.de.
³ State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, PR China.
⁴ Department of Plant Science, The Pennsylvania State University, State College, PA, USA.
⁵ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany.
⁶ Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany.
⁷ College of Resources and Environment, and Academy of Agricultural Sciences, Southwest University (SWU), Chongqing, PR China.
⁸ Laboratorio de Biodiversidad y Funcionamiento Ecosistémico. Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.
⁹ Unidad Asociada CSIC-UPO (BioFun), Universidad Pablo de Olavide, Sevilla, Spain.
¹⁰ Institute of Bio- and Geosciences, Plant Sciences (IBG-2), Forschungszentrum Juelich GmbH, Juelich, Germany.
¹¹ Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany.
¹² Horticultural Sciences Department, University of Florida, Gainesville, FL, USA.
¹³ Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy.
¹⁴ Chair of Root-Soil Interactions, TUM School of Life Sciences, Technical University of Munich, Freising, Germany.
¹⁵ Institute of Bio- and Geosciences, Agrosphere (IBG-3), Forschungszentrum Jülich GmbH, Jülich, Germany.
¹⁶ Earth and Life Institute, Université catholique de Louvain, UCLouvain, Belgium.
¹⁷ Institute of Cellular and Molecular Botany (IZMB), Department of Ecophysiology, University of Bonn, Bonn, Germany.
¹⁸ Intercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, State College, PA, USA.
¹⁹ 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.
²⁰ Plant Breeding, TUM School of Life Sciences, Technical University of Munich, Freising, Germany.
²¹ North Central Regional Plant Introduction Station, USDA-Agriculture Research Service and Iowa State University, Ames, IA, USA.
²² Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany.
²³ Department of Plant Science, The Pennsylvania State University, State College, PA, USA. rjs6686@psu.edu.
²⁴ State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, PR China. wangtianyu@caas.cn.
²⁵ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. hochholdinger@uni-bonn.de.

^# Contributed equally.

PMID: 38778242
DOI: 10.1038/s41588-024-01761-3

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

Peng Yu et al. Nat Genet. 2024 Jun.

. 2024 Jun;56(6):1245-1256.

doi: 10.1038/s41588-024-01761-3. Epub 2024 May 22.

Authors

Affiliations

¹ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. yupeng@uni-bonn.de.
² Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. yupeng@uni-bonn.de.
³ State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, PR China.
⁴ Department of Plant Science, The Pennsylvania State University, State College, PA, USA.
⁵ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany.
⁶ Emmy Noether Group Root Functional Biology, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany.
⁷ College of Resources and Environment, and Academy of Agricultural Sciences, Southwest University (SWU), Chongqing, PR China.
⁸ Laboratorio de Biodiversidad y Funcionamiento Ecosistémico. Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), CSIC, Sevilla, Spain.
⁹ Unidad Asociada CSIC-UPO (BioFun), Universidad Pablo de Olavide, Sevilla, Spain.
¹⁰ Institute of Bio- and Geosciences, Plant Sciences (IBG-2), Forschungszentrum Juelich GmbH, Juelich, Germany.
¹¹ Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany.
¹² Horticultural Sciences Department, University of Florida, Gainesville, FL, USA.
¹³ Department of Agricultural and Food Sciences, University of Bologna, Bologna, Italy.
¹⁴ Chair of Root-Soil Interactions, TUM School of Life Sciences, Technical University of Munich, Freising, Germany.
¹⁵ Institute of Bio- and Geosciences, Agrosphere (IBG-3), Forschungszentrum Jülich GmbH, Jülich, Germany.
¹⁶ Earth and Life Institute, Université catholique de Louvain, UCLouvain, Belgium.
¹⁷ Institute of Cellular and Molecular Botany (IZMB), Department of Ecophysiology, University of Bonn, Bonn, Germany.
¹⁸ Intercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, State College, PA, USA.
¹⁹ 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.
²⁰ Plant Breeding, TUM School of Life Sciences, Technical University of Munich, Freising, Germany.
²¹ North Central Regional Plant Introduction Station, USDA-Agriculture Research Service and Iowa State University, Ames, IA, USA.
²² Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany.
²³ Department of Plant Science, The Pennsylvania State University, State College, PA, USA. rjs6686@psu.edu.
²⁴ State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, PR China. wangtianyu@caas.cn.
²⁵ Crop Functional Genomics, Institute of Crop Science and Resource Conservation (INRES), University of Bonn, Bonn, Germany. hochholdinger@uni-bonn.de.

^# Contributed equally.

PMID: 38778242
DOI: 10.1038/s41588-024-01761-3

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.

PubMed Disclaimer

References

1. Meyer, R. S. & Purugganan, M. D. Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 840–852 (2013). - PubMed
1. Hake, S. & Ross-Ibarra, J. Genetic, evolutionary and plant breeding insights from the domestication of maize. eLife 4, e05861 (2015). - PubMed - PMC
1. Yang, N. et al. Two teosintes made modern maize. Science 382, 1013 (2023).
1. Ross-Ibarra, J. & Piperno, D. Maize moving. Figshare https://doi.org/10.6084/m9.figshare.12781307.v1 (2020).
1. Romero Navarro, J. A. et al. A study of allelic diversity underlying flowering-time adaptation in maize landraces. Nat. Genet. 49, 476–480 (2017). - PubMed

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

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

Affiliations

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

Authors

Affiliations

Abstract

References

MeSH terms

Substances

Grants and funding

LinkOut - more resources

Full Text Sources