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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 Shi1,2, Xue Han2, Xinhao Zhang1, Jie Zhang1, Qi Fu1, Chen Liang1, Fangmeng Duan1, Honghai Zhao1( ), Wenwen Song1( )
College 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
College of Agriculture, Northeast Agricultural University, Harbin 150030, China
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Highlights

  • The m6A modifications reveal distinct post-transcriptional mechanisms in compatible and incompatible soybean–SCN interactions.

  • Incompatible responses exhibit elevated m6A methylation level, more differentially modified peaks and differentially expressed genes (DEGs) than compatible responses.

  • Differentially m6A-modified DEGs are mainly involved in plant–pathogen (compatible) and folate biosynthesis (incompatible) pathways.

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.

References

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Journal of Integrative Agriculture (JIA)
Pages 1875-1891

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Cite this article:
Shi Q, Han X, Zhang X, et al. 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. Journal of Integrative Agriculture (JIA), 2025, 24(5): 1875-1891. https://doi.org/10.1016/j.jia.2023.10.023

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Received: 18 April 2023
Revised: 20 July 2023
Accepted: 11 September 2023
Published: 21 October 2023
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