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Journal of Integrative Agriculture
Journal of Integrative Agriculture  2025, Vol. 24 Issue (2): 453-466    DOI: 10.1016/j.jia.2023.10.039
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A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize
Yang Wang1, 2*, Chunhua Mu3*, Xiangdong Li4, Canxing Duan2, Jianjun Wang5, Xin Lu2, Wangshu Li2, Zhennan Xu2, Shufeng Sun1, 2, Ao Zhang1, Zhiqiang Zhou2, Shenghui Wen5, Zhuanfang Hao2, Jienan Han2, Jianzhou Qu1, Wanli Du1#, Fenghai Li#, Jianfeng Weng2#

1 College of Agronomy, Shenyang Agricultural University, Shenyang 110866, China

2 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China

3 Institute of Maize Research, Shandong Academy of Agricultural Sciences, Jinan 250100, China

4 College of Plant Protection, Shandong Agricultural University, Tai’an 250100, China

5 Institute of Maize, Shanxi Agricultural University, Xinzhou 034000, China

 Highlights 
● Southern corn rust (SCR) resistance loci and candidate genes: A genome-wide association study conducted on 487 diverse inbred maize lines identified 91 loci significantly associated with SCR, including 13 loci that showed significance across at least three environments and overlapped with 74 candidate genes.
● ZmHCT9 associated with SCR resistance: The study identified the candidate gene ZmHCT9, which was upregulated in susceptible inbred lines.  Silencing this gene enhanced resistance to Puccinia polysora, suggesting that ZmHCT9 may act as a negative regulator of resistance to Southern corn rust.
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摘要  

玉米南方锈病（Southern Corn Rust, SCR）是由多堆柄锈菌（Puccinia polysora Underw）引起的气传性真菌病害，在世界范围玉米产区普遍发生，严重影响玉米的产量和品质，而发掘优异抗性位点和候选基因，开展抗病遗传解析，将为解析抗玉米南方锈病抗病育种提供理论参考。本研究以487份温带玉米自交系为材料，利用15,232,270个高质量SNPs结合2021年南宁、2021年三亚和2022年济南三个环境下的玉米南方锈病抗性表型进行全基因组关联分析（Genome wide association study, GWAS），共检测到91个QTLs，其中13个QTLs同时在三个环境被检测到，共涉及94个候选基因（B73_RefGen_v4）。进一步结合转录组测序（RNA sequencing, RNA-seq）分析候选基因，共鉴定到4个候选基因影响玉米南方锈病抗性，其中ZmHCT9编码羟基肉桂酰转移酶，在感病自交系8112中显著上调表达，进一步基于候选基因功能注释，单倍型分析，P. polysora接种后表达量及病毒诱导的基因沉默，发现ZmHCT9负调控玉米南方锈病抗性。



Abstract  
Southern corn rust (SCR) is an airborne fungal disease caused by Puccinia polysora Underw. (P. polysora) that adversely impacts maize quality and yields worldwide.  Screening for new elite SCR-resistant maize loci or genes has the potential to enhance overall resistance to this pathogen.  Using phenotypic SCR resistance-related data collected over two years and three geographical environments, a genome-wide association study was carried out in this work, which eventually identified 91 loci that were substantially correlated with SCR susceptibility.  These included 13 loci that were significant in at least three environments and overlapped with 74 candidate genes (B73_RefGen_v4).  Comparative transcriptomic analyses were then performed to identify the genes related to SCR infection, with 2,586 and 797 differentially expressed genes (DEGs) ultimately being identified in the resistant Qi319 and susceptible 8112 inbred lines following P. polysora infection, respectively, including 306 genes common to both lines.  Subsequent integrative multi-omics investigations identified four potential candidate SCR response-related genes.  One of these genes is ZmHCT9, which encodes the protein hydroxycinnamoyl transferase 9.  This gene was up-regulated in susceptible inbred lines and linked to greater P. polysora resistance as confirmed through cucumber mosaic virus (CMV)-based virus induced-gene silencing (VIGS) system-mediated gene silencing.  These data provide important insights into the genetic basis of the maize SCR response.  They will be useful for for future research on potential genes related to SCR resistance in maize.


Keywords:  maize        southern corn rust        genome-wide association study        transcriptome  
Received: 20 June 2023   Accepted: 28 September 2023
Fund: 
The work was supported by the National Key R&D Program of China (2022YFD1201802), the Shandong Key R&D Program, China (2022CXGC010607), the Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences (CAAS-ZDRW202109), the Sub-project of the Major Project of Science and Technology in Shanxi Province, China (202201140601025-1-02), and the  Agricultural Science and Technology Innovation Project of Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2017-ICS).  We thank Prof. Yule Li (Tsinghua University) and Tao Zhou (China Agricultural University) for providing the VIGS vectors.
About author:  #Correspondence Wanli Du, E-mail: dwl2014@syau.edu.cn; Fenghai Li, E-mail: lifenghai@126.com; Jianfeng Weng, E-mail: wengjianfeng@caas.cn * These authors contributed equally to this study.
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Yang Wang, Chunhua Mu, Xiangdong Li, Canxing Duan, Jianjun Wang, Xin Lu, Wangshu Li, Zhennan Xu, Shufeng Sun, Ao Zhang, Zhiqiang Zhou, Shenghui Wen, Zhuanfang Hao, Jienan Han, Jianzhou Qu, Wanli Du, Fenghai Li, Jianfeng Weng. 2025. A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize. Journal of Integrative Agriculture, 24(2): 453-466.

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