N6-甲基腺苷(m6A)全转录组分析大豆对大豆孢囊线虫亲和性和非亲和性反应揭示了非寄主抗性的特异m6A修饰参与大豆-大豆孢囊线虫的互作

doi:10.1016/j.jia.2023.10.023

Journal of Integrative Agriculture ›› 2025, Vol. 24 ›› Issue (5): 1875-1891.DOI: 10.1016/j.jia.2023.10.023

N⁶-甲基腺苷(m⁶A)全转录组分析大豆对大豆孢囊线虫亲和性和非亲和性反应揭示了非寄主抗性的特异m⁶A修饰参与大豆-大豆孢囊线虫的互作

收稿日期:2023-04-18 修回日期:2023-10-21 接受日期:2023-09-11 出版日期:2025-05-20 发布日期:2025-04-16

Transcriptome-wide N⁶-methyladenosine (m⁶A) profiling of compatible and incompatible responses reveals a nonhost resistance-specific m6A modification involved in soybean–soybean cyst nematode interaction

Qianqian Shi^{1, 2*}, Xue Han^2*, Xinhao Zhang^1*, Jie Zhang¹, Qi Fu¹, Chen Liang¹, Fangmeng Duan¹, Honghai Zhao^1#, Wenwen Song^1#

¹College of Plant Health and Medicine/Engineering Research Center for Precision Pest Management for Fruits and Vegetables of Qingdao/Shandong Engineering Research Center for Environment-Friendly Agricultural Pest Management, Qingdao Agricultural University, Qingdao 266109, China
²College of Agriculture, Northeast Agricultural University, Harbin 150030, China

Received:2023-04-18 Revised:2023-10-21 Accepted:2023-09-11 Online:2025-05-20 Published:2025-04-16
About author:Qianqian Shi, E-mail: shiqianqian@qau.edu.cn; #Correspondence Honghai Zhao, E-mail: hhzhao@qau.edu.cn; Wenwen Song, E-mail: wwsong@qau.edu.cn * These authors contributed equally to this study.
Supported by:
This study is supported by the National Natural Science Foundation of China (31901858 and 31901859).

摘要/Abstract

摘要：

大豆孢囊线虫（Soybean cyst nematode, SCN; Heterodera glycines）是世界范围内最具破坏性的大豆病原物之一。研究大豆-SCN互作机制对提出新的病害防控策略、培育抗大豆孢囊线虫病的大豆新品种具有重要实践意义。SCN侵染可诱导大豆的多个差异基因上调或下调表达。然而，差异基因表达变化的调控机制在很大程度上仍未被探索。N⁶ -甲基腺苷（m⁶A）甲基化是最广泛存在的mRNA修饰之一，在植物响应病原物侵染过程中发挥重要的转录重编程的调控作用。然而，在大豆对SCN的亲和性和非亲和性反应中是否也存在m⁶A甲基化对差异基因的表达调控作用尚未明确。为此，本研究首先明确了大豆品种Williams 82 对SCN race 3具有敏感性（亲和性反应），但对SCN_T（大豆孢囊线虫烟草群体）存在非寄主抗性（非亲和性反应）；其次通过液相色谱-串联质谱法检测了m⁶A/A比率。结果表明，与亲和性反应相比，m⁶A甲基化整体水平在非亲和性反应中显著升高；在此基础上，通过N⁶-甲基腺苷(m⁶A)全转录组比较了大豆对SCN的亲和性和非亲和性反应的差异。在非亲和性反应中，差异修饰m⁶A峰（differentially modified m⁶A peaks, DMPs）和差异表达基因（differentially expressed genes, DEGs）的数量均显著增多；在亲和反应和非亲和反应中，分别存在133和194个差异表达基因的m⁶A甲基化修饰水平也表现出差异显著性 (我们将这些基因称为DMDs)。亲和反应中的DMDs显著富集在玉米素生物合成、植物-病原互作、糖酵解/糖异生和醚脂质代谢途径，且与植物-病原互作途径相关的DMDs表达量下调最多；而与SCN_T侵染的非亲和反应中仅叶酸生物合成通路被显著富集，且该通路的DMDs表达量上调最多。综上所述，本研究首次明确了大豆-SCN互作中存在m⁶A甲基化修饰，且m⁶A全转录组在大豆和SCN的亲和和非亲和反应中存在差异。研究结果为大豆-SCN的非寄主抗性反应在转录后修饰水平上的调控机制提供了新的见解，对提高大豆抗SCN育种有重要应用价值。

Abstract:

Soybean cyst nematode (SCN, Heterodera glycines) is a devastating pathogen that infects soybean (Glycine max L. Merrill) and disrupts soybean production worldwide. SCN infection upregulates or downregulates the expression of multiple genes in soybean. However, the regulatory mechanisms that underlie these changes in gene expression remain largely unexplored. N⁶-methyladenosine (m⁶A) methylation, one of the most prevalent mRNA modifications, contributes to transcriptional reprogramming during plant responses to pathogen infection. Nevertheless, the role of m⁶A methylation in establishing compatible and incompatible soybean responses to SCN has not previously been studied. Here, we performed transcriptome-wide m⁶A profiling of soybean roots infected with virulent and avirulent populations of SCN. Compared with the compatible response, the incompatible response was associated with higher global m⁶A methylation levels, as well as more differentially modified m⁶A peaks (DMPs) and differentially expressed genes (DEGs). A total of 133 and 194 genes showed significant differences in both transcriptional expression and m⁶A methylation levels in compatible and incompatible interactions; the most significantly enriched gene ontology terms associated with these genes were plant–pathogen interaction (compatible) and folate biosynthesis (incompatible). Our findings demonstrate that the m⁶A methylation profiles of compatible and incompatible soybean responses are distinct and provide new insights into the regulatory mechanism underlying soybean response to SCN at the post-transcriptional modification level, which will be valuable for improving the SCN-resistant breeding.

Key words: N⁶-methyladenosine , soybean cyst nematode , MeRIP-seq , RNA-seq

Qianqian Shi, Xue Han, Xinhao Zhang, Jie Zhang, Qi Fu, Chen Liang, Fangmeng Duan, Honghai Zhao, Wenwen Song.

N⁶-甲基腺苷(m⁶A)全转录组分析大豆对大豆孢囊线虫亲和性和非亲和性反应揭示了非寄主抗性的特异m⁶A修饰参与大豆-大豆孢囊线虫的互作 [J]. Journal of Integrative Agriculture, 2025, 24(5): 1875-1891.

Qianqian Shi, Xue Han, Xinhao Zhang, Jie Zhang, Qi Fu, Chen Liang, Fangmeng Duan, Honghai Zhao, Wenwen Song. Transcriptome-wide N⁶-methyladenosine (m⁶A) profiling of compatible and incompatible responses reveals a nonhost resistance-specific m6A modification involved in soybean–soybean cyst nematode interaction[J]. Journal of Integrative Agriculture, 2025, 24(5): 1875-1891.

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N⁶-甲基腺苷(m⁶A)全转录组分析大豆对大豆孢囊线虫亲和性和非亲和性反应揭示了非寄主抗性的特异m⁶A修饰参与大豆-大豆孢囊线虫的互作

Transcriptome-wide N⁶-methyladenosine (m⁶A) profiling of compatible and incompatible responses reveals a nonhost resistance-specific m6A modification involved in soybean–soybean cyst nematode interaction

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