Genetic dissection of maize kernel protein content through a multi-locus genome-wide association study

doi:10.1016/j.jia.2025.06.016

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Jihong Zhang¹^*, Na Liu^1,²^*, Shiwei Wang¹, Xiang Guo¹, Xinyu Sun¹, Haiyang Duan¹, Lianglei Zhang¹, Liang Yuan¹, Huiling Xie¹, Huili Yang¹, Xiaoyang Chen¹, Dong Ding¹, Jihua Tang^1,³^#, Xuehai Zhang¹^#

¹State Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping/College of Agronomy, Henan Agricultural University, Zhengzhou 450046, China

²College of Biological Engineering, Henan University of Technology, Zhengzhou 450001, China

³The Shennong Laboratory, Zhengzhou 450002, China

Highlights

1. A genome-wide association study (GWAS) integrating six models identified 473 QTNs and 115 co-localized loci associated with kernel protein content (PC) in maize, with the 3VmrMLM model detecting the most QTNs.

2. The candidate gene Zm00001d037565, encoding GA2-oxidase, exhibited strong selection signals during maize domestication and breeding.

3. A favorable haplotype (HapA) of Zm00001d037565 significantly increased kernel PC, making it a promising target for high-protein maize breeding.

Abstract
References

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摘要

玉米籽粒蛋白质含量（Protein Content, PC）是决定其营养品质的重要指标，但其遗传基础尚未被充分解析。本研究以264份玉米自交系为材料，利用125万个单核苷酸多态性标记，综合应用BLINK、FarmCPU、MLM、MLMM、SUPER和3VmrMLM等六种分析模型开展了其籽粒PC的全基因组关联分析。结果表明，籽粒PC在不同材料间表现出较大变异，范围为9.26%至20.94%，广义遗传力为0.56。共检测到473个显著的数量性状核苷酸（Quantitative trait nucleotides, QTN），每个QTN对表型变异的解释率在0.08%至7.10%之间。其中，有115个QTNs在不同模型、环境和分析方法下重复被检测到。值得注意的是，3VmrMLM模型检测到的显著QTNs数量最多（59个），其中38个表现出基因型×环境互作效应；而MLM模型检测到的显著QTNs数量最少，仅为8个。进一步分析共鉴定出35个候选基因，位于显著QTN邻近区域或其上。其中，Zm00001d033805、Zm00001d037565、Zm00001d052164和Zm00001d031535等四个基因与籽粒PC密切相关，涉及氮代谢、光合作用和三羧酸循环等关键生物过程。特别地，编码赤霉素2-氧化酶的Zm00001d037565在籽粒发育中发挥作用，可能参与调控籽粒蛋白质的积累。单倍型分析显示，该基因的HapA型与较高的PC显著相关。选择扫描分析表明，该基因在玉米从祖先类群（Zea mays ssp. mexicana和Zea mays ssp. parviglumis）驯化为栽培种、从热带/亚热带区域向温带区域适应，以及现代育种过程中均受到了选择。综上，本研究加深了对玉米籽粒蛋白质含量遗传机制的理解，提供了可用于分子育种的关键基因资源和靶标，为高蛋白玉米的选育提供了新思路和理论支撑。

Abstract

Protein content (PC) in maize kernels is a key determinant of their nutritional quality, however, its genetic basis remains largely unexplored. In this study, we conducted a genome-wide association study (GWAS) using 264 maize inbred lines and 1.25 million single nucleotide polymorphisms (SNPs), applying six GWAS models: BLINK, FarmCPU, MLM, MLMM, SUPER, and 3VmrMLM. Kernel PC exhibited substantial variation, ranging from 9.26 to 20.94%, with a broad-sense heritability of 0.56. A total of 473 significant quantitative trait nucleotides (QTNs) were detected, each explaining 0.08 to 7.10% of the phenotypic variance. Among them, 115 QTNs were consistently detected across different models, environments and analytical methods. Notably, 3VmrMLM model identified 59 most significant QTNs, with 38 were QEIs, and the MLM model identified the fewest significant QTNs (8). We further identified 35 candidate genes located within or adjacent to the significant QTNs. Among these, four genes - Zm00001d033805, Zm00001d037565, Zm00001d052164 and Zm00001d031535 - were strongly associated with PC. These genes are implicated in critical biological pathways, including nitrogen metabolism, photosynthesis, and the tricarboxylic acid (TCA) cycle. Notably, Zm00001d037565, encoding a gibberellin 2-oxidase, plays a role in seed development and is likely involved in regulating protein accumulation in kernels. Haplotype analysis revealed that the HapA of Zm00001d037565 is significantly associated with higher PC. Selective sweep analysis indicated that this gene underwent selection during maize domestication from teosinte (Zea mays ssp. mexicana and Zea mays ssp. parviglumis), its adaptation from tropical/subtropical to temperate regions, and throughout modern breeding programs. Overall, this study advances our understanding of the genetic architecture of maize kernel PC and provides valuable candidate genes and haplotypes for marker-assisted selection, offering new targets for developing high-protein maize varieties.

Keywords: maize protein content GWAS multi-Models 3VmrMLM

Online: 09 June 2025

Fund:

This research was supported by the National Key Research and Development Program of China (2021YFF1000300), the Special Project of Key Research and Development Program of Henan Province, China (251111111000), the Henan Province Science and Technology Attack Project, China (242102110307 and 232102110181), and the Henan Provincial Higher Education Key Research Project, China (24B210003).

About author: #Correspondence Xuehai Zhang, Tel: +86-371-56990188, Fax: +86-371-56990186, E-mail: xuehai85@126.com; Jihua Tang, E-mail: tangjihua1@163.com * These authors contributed equally to this manuscript.

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Jihong Zhang, Na Liu, Shiwei Wang, Xiang Guo, Xinyu Sun, Haiyang Duan, Lianglei Zhang, Liang Yuan, Huiling Xie, Huili Yang, Xiaoyang Chen, Dong Ding, Jihua Tang, Xuehai Zhang. 2025. Genetic dissection of maize kernel protein content through a multi-locus genome-wide association study. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.06.016

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