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Genome-wide dissection of changes in maize root system architecture during modern breeding

Nature Plants volume 8, pages 1408–1422 (2022)Cite this article

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Abstract

Appropriate root system architecture (RSA) can improve maize yields in densely planted fields, but little is known about its genetic basis in maize. Here we performed root phenotyping of 14,301 field-grown plants from an association mapping panel to study the genetic architecture of maize RSA. A genome-wide association study identified 81 high-confidence RSA-associated candidate genes and revealed that 28 (24.3%) of known root-related genes were selected during maize domestication and improvement. We found that modern maize breeding has selected for a steeply angled root system. Favourable alleles related to steep root system angle have continuously accumulated over the course of modern breeding, and our data pinpoint the root-related genes that have been selected in different breeding eras. We confirm that two auxin-related genes, ZmRSA3.1 and ZmRSA3.2, contribute to the regulation of root angle and depth in maize. Our genome-wide identification of RSA-associated genes provides new strategies and genetic resources for breeding maize suitable for high-density planting.

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Fig. 1: Changes in RSA over the course of Chinese maize breeding.
Fig. 2: GWAS identification of candidate genes for variation in maize root traits.
Fig. 3: Profiling of selective sweeps during maize domestication, improvement and modern breeding.
Fig. 4: The role of favourable alleles in the maize breeding process.
Fig. 5: Validation of two candidate genes associated with RSA.
Fig. 6: Genes that have been reported to affect the development of maize roots.

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Data availability

Data supporting the findings of this work are available within the paper and its Supplementary Information. The genotype set, population structure and kinship data can be downloaded from the Maizego website (http://www.maizego.org/Resources.html). All root phenotype data for the 380 inbred maize lines are included in Supplementary Table 25. The RNA-sequencing reads used to construct the co-expression network and the root transcriptome sequencing reads were deposited in the NCBI Sequence Read Archive (https://www.ncbi.nlm.nih.gov/) under accession codes PRJNA694491 and PRJNA693427, respectively. Source data are provided with this paper.

Code availability

All scripts for GWAS, co-expression network analysis, selective sweep detection for domestication and improvement, and obtaining aligned sequences of high-priority candidate genes and known root-related genes (https://doi.org/10.5281/zenodo.7112683) are available on Zenodo.

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Acknowledgements

This study was financially supported by the National Key Research and Development Program of China (grant nos. 2021YFF1000500 (Q.P.), 2021YFD1200700 (F.C.) and 2016YFD0100700 (L.Y.)), the National Natural Science Foundation of China (grant nos. 31972485 (F.C.) and 31971948 (Q.P.)), the Hainan Natural Science Foundation Innovation Research Team Project (grant no. 321CXTD443 (F.C.)), the Hainan Provincial Science and Technology Plan Sanya Yazhou Bay Science and Technology City Joint Project (grant no. 320LH011 (Q.P.)) and the China Postdoctoral Science Foundation (grant no. 2021M693431 (W.R.)). The transgenic maize seeds were produced by the Center for Crop Functional Genomics and Molecular Breeding of China Agricultural University.

Author information

Authors and Affiliations

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

    Wei Ren, Longfei Zhao, Jiaxing Liang, Pengcheng Li, Zhigang Liu, Xiaojie Li, Zhihai Zhang, Jieping Li, Kunhui He, Zheng Zhao, Guohua Mi, Fusuo Zhang, Fanjun Chen, Lixing Yuan & Qingchun Pan

  2. Cereal Crops Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou, China

    Lifeng Wang

  3. Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing, China

    Limei Chen & Lixing Yuan

  4. Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou, China

    Pengcheng Li

  5. Cereal Crops Research Institute, Pirsabak, Nowshera, Pakistan

    Farhan Ali

  6. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    Jianbing Yan

  7. Sanya Institute of China Agricultural University, Sanya, China

    Fanjun Chen & Qingchun Pan

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  1. Wei Ren
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Contributions

Q.P., L.Y. and F.C. conceived and designed the research. W.R., L.Z., J. Liang, L.W., P.L., Z.L., X.L., Z. Zhang and J. Li performed phenotypic measurements. W.R. and Q.P. performed the data analyses. L.C. performed plasmid construction and genetic transformation. W.R., K.H. and Z. Zhao characterized the transgenic overexpression lines. J.Y. provided the maize inbred lines and genotype set. W.R. and Q.P. wrote the manuscript. F.A., G.M., J.Y., F.Z., F.C., L.Y. and Q.P. revised the manuscript. All authors contributed to the final version of the paper.

Corresponding authors

Correspondence to Fanjun Chen, Lixing Yuan or Qingchun Pan.

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The authors declare no competing interests.

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Nature Plants thanks Yusaku Uga, Ana Letycia Basso Garcia, Ana Caño-Delgado and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Pearson correlations among eight root traits.

The red lines represent positive correlations, and the green lines represent negative correlations. The line width represents the strength of the correlation. Yellow lines indicate that the correlation coefficient was close to zero.

Source data

Extended Data Fig. 2 Principal component analysis of eight root traits.

The red ellipse indicates the area-related traits; the yellow ellipse indicates the width-related traits; and the green ellipse indicates the angle-related traits.

Extended Data Fig. 3 Cluster analysis of 380 maize inbred lines based on root traits.

(a) Cluster analysis of 380 inbred lines based on ROA, RMEW, and AREA. (b) Representative inbred lines from the three clusters (groups 1–3). (c) Comparison of eight root traits among groups 1–3. (d) Comparison of eight root traits among four subpopulations. (e) Proportion of lines from each of four subgroups in the three cluster groups. The four subgroups (Mixed, SS, NSS, and TST) are based on genetic relationships among the different inbred lines. Mixed, mixed group; SS, stiff stalk group; NSS, non-stiff stalk group; TST, tropical and subtropical group.

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Supplementary Table 28

Supplementary Tables 1–28.

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Ren, W., Zhao, L., Liang, J. et al. Genome-wide dissection of changes in maize root system architecture during modern breeding. Nat. Plants 8, 1408–1422 (2022). https://doi.org/10.1038/s41477-022-01274-z

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