Genome-wide DNA methylation landscape and its association with the transcriptome reprogramming in potato in response to Phytophthora infestans infection

Abstract

Late blight, caused by the oomycete Phytophthora infestans, is one of the most destructive diseases affecting potato production globally. However, the function of DNA methylation (DNAm) and its association with simultaneous alteration in gene expression in potato’s response to P. infestans infection remain largely unknown. Here, we conducted whole-genome bisulfite sequencing and RNA sequencing on potato cultivar Qingshu No.9 inoculated with P. infestans. Significantly, we identified 18 119 differentially expressed genes (DEGs) across at least one of the four post-inoculation time points. A few pathogenesis-related (PR) genes involved in salicylic acid, ethylene signaling, and DNAm regulation exhibited activation at early infection stages, although they were predominantly downregulated after the onset of necrosis in plants. Hypomethylation changes at 12 h post-inoculation (hpi) were followed by hypermethylation at 24 hpi, with CHH methylation being the primary factor influencing the DNAm pattern. Differentially methylated regions (DMRs) showed significant enrichment at DEGs. Specially, DNAm variations could be associated with subsequent transcriptional changes. This is exemplified by 24 h-hyper-CHG methylation at the gene body that correlates with expression downregulation at 48 hpi, including genes involved in chromatin remodeling pathways. Furthermore, we observed a significant enrichment of hypomethylation changes at the exon of NB-LRR genes, which ultimately resulted in their downregulation. In summary, we have elucidated the DNAm pattern of potato in response to infection by P. infestans, and identified the involvement of epigenetic mechanisms in the reprogramming of the transcriptome, which ultimately contributed to the suppression of immunity and the development of potato late blight.

Acknowledgements

We thank Dr. Tengbo Huang (Shenzhen University, China) for helpful discussions and suggestions on the manuscript. We thank the High-Performance Computing platform of Northwest A&F University for providing computing resources. This project was supported by the National Key R&D Program of China (2023YFD2302100), the PhD Start-up Fund of Northwest A&F University (grant no. Z1090122063), the open fund of Guangdong Provincial Key Laboratory for Plant Epigenetics (GPKLPE202414), the China Agriculture Research System (CARS-09).

Authors contributions

P.T. and W.S. designed the experiments. J.Z., B.W., W.J., J.S., Z.M., P.H., H.Z., and Y.M. conducted the experiments, P.T. analyzed the data. P.T., Y.S., and W.S. wrote the article. All authors read and approved the final manuscript.

Data availability

The data of this study was submitted to National Genomics Data Center (https://ngdc.cncb.ac.cn/) under the project number PRJCA031393, with the RNA-seq raw reads under the GSA accession CRA019840, and the raw bisulfite-seq reads under CRA019846.

Conflicts of interest statement

The authors declare no conflicts of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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