The fungicide pyraclostrobin affects gene expression by altering the DNA methylation pattern in Magnaporthe oryzae

Shumei Fang; Hanxin Wang; Kaihua Qiu; Yuanyuan Pang; Chen Li; Xilong Liang

doi:10.3389/fpls.2024.1391900

The fungicide pyraclostrobin affects gene expression by altering the DNA methylation pattern in Magnaporthe oryzae

Front Plant Sci. 2024 Apr 30:15:1391900. doi: 10.3389/fpls.2024.1391900. eCollection 2024.

Authors

Shumei Fang^{1

2}, Hanxin Wang², Kaihua Qiu¹, Yuanyuan Pang², Chen Li¹, Xilong Liang¹

Affiliations

¹ Heilongjiang Plant Growth Regulator Engineering Technology Research Center, College of Agriculture, Heilongjiang Bayi Agricultural University, Daqing, China.
² Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in Cold Region, College of Life Science and Biotechnology, Heilongjiang Bayi Agricultural University, Daqing, China.

Abstract

Introduction: Rice blast disease caused by Magnaporthe oryzae has long been the main cause of rice (Oryza sativa L.) yield reduction worldwide. The quinone external inhibitor pyraclostrobin is widely used as a fungicide to effectively control the spread of pathogenic fungi, including M. oryzae. However, M. oryzae can develop resistance through multiple levels of mutation, such as target protein cytb mutation G143A/S, leading to a decrease in the effectiveness of the biocide after a period of application. Therefore, uncovering the possible mutational mechanisms from multiple perspectives will further provide feasible targets for drug development.

Methods: In this work, we determined the gene expression changes in M. oryzae in response to pyraclostrobin stress and their relationship with DNA methylation by transcriptome and methylome.

Results: The results showed that under pyraclostrobin treatment, endoplasmic reticulum (ER)-associated and ubiquitin-mediated proteolysis were enhanced, suggesting that more aberrant proteins may be generated that need to be cleared. DNA replication and repair processes were inhibited. Glutathione metabolism was enhanced, while lipid metabolism was impaired. The number of alternative splicing events increased. These changes may be related to the elevated methylation levels of cytosine and adenine in gene bodies. Both hypermethylation and hypomethylation of differentially methylated genes (DMGs) mainly occurred in exons and promoters. Some DMGs and differentially expressed genes (DEGs) were annotated to the same pathways by GO and KEGG, including protein processing in the ER, ubiquitin-mediated proteolysis, RNA transport and glutathione metabolism, suggesting that pyraclostrobin may affect gene expression by altering the methylation patterns of cytosine and adenine.

Discussion: Our results revealed that 5mC and 6mA in the gene body are associated with gene expression and contribute to adversity adaptation in M. oryzae. This enriched the understanding for potential mechanism of quinone inhibitor resistance, which will facilitate the development of feasible strategies for maintaining the high efficacy of this kind of fungicide.

Keywords: Magnaporthe oryzae; adenine methylation; cytosine methylation; gene expression; pyraclostrobin.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by Incubation Subjects of Heilongjiang Bayi Agricultural University [grant number XZR2014-01], the Provincial and Natural Science Foundation of Heilongjiang, China [grant number C2016047] and PhD research startup foundation of Heilongjiang Bayi Agricultural University [XDB-2016-01].