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Hybrid performance evaluation and genome-wide association analysis of root system architecture in a maize association population

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Abstract

Key Message

The genetic architecture of RSA traits was dissected by GWAS and coexpression networks analysis in a maize association population.

Abstract

Root system architecture (RSA) is a crucial determinant of water and nutrient uptake efficiency in crops. However, the maize genetic architecture of RSA is still poorly understood due to the challenges in quantifying root traits and the lack of dense molecular markers. Here, an association mapping panel including 356 inbred lines were crossed with a common tester, Zheng58, and the test crosses were phenotyped for 12 RSA traits in three locations. We observed a 1.3 ~ sixfold phenotypic variation for measured RSA in the association panel. The association panel consisted of four subpopulations, non-stiff stalk (NSS) lines, stiff stalk (SS), tropical/subtropical (TST), and mixed. Zheng58 × TST has a 2.1% higher crown root number (CRN) and 8.6% less brace root number (BRN) than Zheng58 × NSS and Zheng58 × SS, respectively. Using a genome-wide association study (GWAS) with 1.25 million SNPs and correction for population structure, 191 significant SNPs were identified for root traits. Ninety (47%) of the significant SNPs showed positive allelic effects, and 101 (53%) showed negative effects. Each locus could explain 0.39% to 11.8% of phenotypic variation. By integrating GWAS results and comparing coexpression networks, 26 high-priority candidate genes were identified. Gene GRMZM2G377215, which belongs to the COBRA-like gene family, affected root growth and development. Gene GRMZM2G468657 encodes the aspartic proteinase nepenthesin-1, related to root development and N-deficient response. Collectively, our research provides progress in the genetic dissection of root system architecture. These findings present the further possibility for the genetic improvement of root traits in maize.

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Data availability

The genotype data for the association panel are available at http://www.maizego.org/Resources.html. All other data supporting the findings of this study are available within the paper, and its supplementary data is published online.

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Acknowledgements

The authors gratefully acknowledge Dr. Jianbin Yan, Huazhong Agricultural University, who provided the germplasm resources and established the genotypes for the association mapping population.We also thank Dr. Philip James Kear, from International Potato Center–China Center for Asia and the Pacific, for providing valuable feedback and editing the revised version of our manuscript.

Funding

This study was financially supported by the Hainan Provincial Natural Science Foundation of China (321CXTD443) and the National Natural Science Foundation of China (31972485, 31971948).

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Authors and Affiliations

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

    Zhigang Liu, Wei Ren, Guohua Mi, Lixing Yuan, Fanjun Chen & Qingchun Pan

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

    Pengcheng Li

  3. College of Resources and Environment, Jilin Agricultural University, Changchun, China

    Zhe Chen

  4. Global Institute for Food Security, University of Saskatchewan, Saskatoon, Canada

    Zhigang Liu & Toluwase Olukayode

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

    Fanjun Chen & Qingchun Pan

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  1. Zhigang Liu
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Contributions

FC and QP designed the experiment; ZL analyzed the data and wrote the manuscript; PL performed the experiments; WR and ZC assisted in data analysis; and OT, GM, LY, FC, and QP contributed to manuscript editing.

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Correspondence to Qingchun Pan.

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122_2023_4442_MOESM1_ESM.xlsx

Supplement Table S1: Information of the 356 representative maize panel. Supplement Table S2: Environmental information of Guangxing, Yunnan and Hainan locations for field experiments in this study. Supplement Table S3: Summary of the significant SNPs association loci for root traits. (XLSX 43 KB)

122_2023_4442_MOESM2_ESM.tif

Supplement Figure 1 Distribution of 1.25 million polymorphic SNPs in the maize genome. Heatmap of SNP density on the chromosome within a 1-Mb interval, colors were used to indicate the number of SNPs within the 1-Mb interval. The physical position of the SNPs was based on the B73 reference sequence (RefGen_V2). (TIF 9090 KB)

122_2023_4442_MOESM3_ESM.tif

Supplement Figure 2 Distribution and correlation of root system architecture traits between each pair of locations. The significance levels of pairwise t-tests were added. * indicates P ≤ 0.05, ** indicates P ≤ 0.01; *** indicates P ≤ 0.001; **** indicates P ≤ 0.0001. Different lowercase letters indicate significant differences (P < 0.05) in different locations, as determined by Tukey's HSD test. Abbreviations for root traits are as follows: BRN, brace root number; BRWN, brace root whorl number; CR1, 1st whorl crown roots; CR2, 2nd whorl crown roots; CR3, 3rd whorl crown roots; CR4, 4th whorl crown roots; CR5, 5th whorl crown roots; CR6, 6th-8th whorl crown roots; CRN, crown root number; CRWN, crown root whorl number; NRWN, nodal root whorl number. GX11: Guangxi location in 2011, HN11: Hainan location in 2011, YN11: Yunnan location in 2011. (TIF 9318 KB)

122_2023_4442_MOESM4_ESM.tif

Supplement Figure 3 The phenotypic distribution of root traits in the association panel. Abbreviations for root traits are as follows: BRN, brace root number; BRWN, brace root whorl number; CR1, 1st whorl crown roots; CR2, 2nd whorl crown roots; CR3, 3rd whorl crown roots; CR4, 4th whorl crown roots; CR5, 5th whorl crown roots; CR6, 6th-8th whorl crown roots; CRN, crown root number; CRWN, crown root whorl number; NRWN, nodal root whorl number. (TIF 65415 KB)

122_2023_4442_MOESM5_ESM.tif

Supplement Figure 4 Phenotypic correlations among the root traits in the association panel. Abbreviations for root traits are as follows: BRN, brace root number; BRWN, brace root whorl number; CR1, 1st whorl crown roots; CR2, 2nd whorl crown roots; CR3, 3rd whorl crown roots; CR4, 4th whorl crown roots; CR5, 5th whorl crown roots; CR6, 6th-8th whorl crown roots; CRN, crown root number; CRWN, crown root whorl number; NRWN, nodal root whorl number. (TIF 61613 KB)

122_2023_4442_MOESM6_ESM.tif

Supplement Figure 5 The percentage of total variance explained by each principal component. Abbreviations for root traits are as follows: BRN, brace root number; BRWN, brace root whorl number; CR1, 1st whorl crown roots; CR2, 2nd whorl crown roots; CR3, 3rd whorl crown roots; CR4, 4th whorl crown roots; CR5, 5th whorl crown roots; CR6, 6th-8th whorl crown roots; CRN, crown root number; CRWN, crown root whorl number; NRN, nodal root number; NRWN, nodal root whorl number. (TIF 11460 KB)

122_2023_4442_MOESM7_ESM.tif

Supplement Figure 6 Comparison of root traits between PA and SPT heterotic groups. Different lowercase letters indicate significant differences (P < 0.05) in different locations, as determined by Tukey's HSD test. Abbreviations for root traits are as follows: BRN, brace root number; BRWN, brace root whorl number; CR1, 1st whorl crown roots; CR2, 2nd whorl crown roots; CR3, 3rd whorl crown roots; CR4, 4th whorl crown roots; CR5, 5th whorl crown roots; CR6, 6th-8th whorl crown roots; CRN, crown root number; CRWN, crown root whorl number; NRN, nodal root number; NRWN, nodal root whorl number. (TIF 11656 KB)

122_2023_4442_MOESM8_ESM.tif

Supplement Figure 7 Quantile–quantile plots of root traits. (a) BRN, brace root number, (b) BRWN, brace root whorl number, (c) CR1, 1st whorl crown roots, (d) CR2, 2nd whorl crown roots, (e) CR3, 3rd whorl crown roots, (f) CR4, 4th whorl crown roots, (g) CR5, 5th whorl crown roots, (h) CR6, 6th-8th whorl crown roots, (i) CRN, crown root number, (j) CRWN, crown root whorl number, (k) NRN, nodal root number, (l) NRWN, nodal root whorl number. (TIF 60252 KB)

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Liu, Z., Li, P., Ren, W. et al. Hybrid performance evaluation and genome-wide association analysis of root system architecture in a maize association population. Theor Appl Genet 136, 194 (2023). https://doi.org/10.1007/s00122-023-04442-7

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  • DOI: https://doi.org/10.1007/s00122-023-04442-7

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