Accumulation of beneficial haplotypes in the Huang-Huai-Hai wheat region and its application in molecular breeding

doi:10.1016/j.jia.2024.12.003

Journal of Integrative Agriculture

2026, Vol. 25

Issue (10): 4014-4026 DOI: 10.1016/j.jia.2024.12.003

Crop Science

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Accumulation of beneficial haplotypes in the Huang-Huai-Hai wheat region and its application in molecular breeding

Chengzhi Jiao¹^*, Mingxing Wen¹^*, Xin Jing², Vanika Garg³, Chuanqing Zhou², Liyang Chen², Fengfeng Xu², Chenyang Hao⁴, Jin Xiao¹, Haiyan Wang¹, Rajeev K. Varshney³, Xueyong Zhang⁴, Xiu’e Wang^1#

¹State Key Laboratory of Crop Genetics and Germplasm Enhancement & Utilization/Zhongshan Biological Breeding Laboratory/Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing 210095, China

²Smartgenomics Technology Institute, Tianjin 301700, China

³Centre for Crop & Food Innovation/WA State Agricultural Biotechnology Centre/Food Futures Institute, Murdoch University, Murdoch 6150, Australia

⁴National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China

Highlights
● The Huang-Huai-Hai wheat region (HHHR) shows superior yields and disease resistance, and beneficial haplotypes are more frequent than in other regions.
● The MFP-a gene may affect both grain development and powdery mildew resistance.
● Identity by descent analysis identified fixed genomic segments in HHHR, which can aid breeding targets.

Abstract
References

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摘要

黄淮海麦区是我国种植面积最大、产量最高的小麦主产区。在我国70年的育种历史中，黄淮海麦区小麦育种成绩突出，育成一系列高产、稳产、抗病品种，但目前对该区域小麦育种进程中组学层面的研究还不够系统。本研究利用55K SNP芯片（Affymetrix® Axiom® Wheat55K）对387份来自不同麦区的小麦种质进行基因型扫描，并整合了476份种质660K SNP芯片（Affymetrix® Axiom® Wheat660K）基因型数据和145份种质的重测序基因型数据，系统地分析了黄淮麦区小麦品种的产量、抗白粉病等性状的表型以及优异等位基因的分布规律。结果发现，黄淮麦区小麦品种的产量相关性状和白粉病抗性显著高于其他麦区品种；通过全基因组关联分析（genome-wide association study，GWAS）鉴定到了与产量和抗白粉病相关的数量性状遗传位点（quantitative trait nucleotides，QTN），这些性状的优异单倍型在黄淮麦区的累计频率显著高于其他麦区。发现产量和抗性共定位的一个位点，其中一个茉莉酸合成MFP-a基因与小麦籽粒发育和抗白粉病性均显著关联。通过同源一致性分析（identity by descent，IBD）鉴定到了黄淮麦区育种正向选择、固定下来的基因组区段，可用来定向改良其他麦区的产量和抗病性状，以矮孟牛育种系谱为例，解析了重要育种骨干亲本形成的遗传学基础，为小麦分子育种提供了参考。

Abstract

The Huang-Huai-Hai wheat region (HHHR) is characterized by the largest cultivation area and highest yield among all the major wheat-producing regions in China. Over the past 70 years, significant advances in wheat breeding have been achieved in this region, resulting in high and stable yields as well as improved disease resistance. However, a notable deficiency remains in the systematic molecular-level analyses of wheat breeding advantages in HHHR. To bridge this gap, we used a Wheat 55K SNP array to evaluate 384 accessions from a core collection of wheat germplasms across China, and then systematically analyzed the distribution patterns of beneficial haplotypes associated with traits related to yield and powdery mildew resistance specific to HHHR. The findings indicate that varieties from HHHR demonstrate significantly superior performance in terms of yield-related traits and powdery mildew resistance compared to those from other wheat regions. A genome-wide association study (GWAS) analysis identified the quantitative trait nucleotides (QTNs) associated with both grain yield and powdery mildew resistance. Importantly, beneficial haplotypes were found at significantly higher frequencies in the HHHR than in other wheat-growing regions. Based on these haplotypes, the MFP-a gene was identified as potentially regulating jasmonic acid synthesis while also playing a role in grain development and conferring powdery mildew resistance. Furthermore, identity by descent (IBD) analysis revealed specific conserved genomic segments that have become fixed through selective breeding practices in HHHR, which may serve as valuable resources for the targeted enhancement of yield and disease resistance traits in other wheat-growing areas. Finally, the Aimengniu breeding lineage was used as a case study to elucidate the genetic basis underlying the key founder parental formations utilized in breeding programs. This study not only provides essential references and guidance for future molecular breeding initiatives in China but also has implications for enhancing wheat production worldwide.

Keywords: wheat breeding HHHR yield powdery mildew resistance GWAS IBD

Received: 28 October 2024 Accepted: 08 November 2024 Online: 04 December 2024

Fund:

This project was supported by the Zhongshan Biological Breeding Laboratory, Jiangsu Province, China (ZSBBL-KY2023-02-2), the National Key Research and Development Program of China (2023YFF1000603), the Jiangsu Provincial Key Research and Development Program, China (BE2022346 and BE2023313), the Seed Industry Revitalization Project of Jiangsu Province, China (JBGS (2021) 006, JBGS (2021) 047), the Jiangsu Agricultural Technology System, China (JATS[2023]422), and the Joint Research of Wheat Variety Improvement of Anhui Province, China (2021-2025).

About author: #Correspondence Xiu’e Wang, E-mail: xiuew@njau.edu.cn * These authors contributed equally to this study.

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Chengzhi Jiao, Mingxing Wen, Xin Jing, Vanika Garg, Chuanqing Zhou, Liyang Chen, Fengfeng Xu, Chenyang Hao, Jin Xiao, Haiyan Wang, Rajeev K. Varshney, Xueyong Zhang, Xiu’e Wang. 2026. Accumulation of beneficial haplotypes in the Huang-Huai-Hai wheat region and its application in molecular breeding. Journal of Integrative Agriculture, 25(10): 4014-4026.

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