Abstract
Key message
This study provided important insights into the complex epigenetic regulatory of H3K9ac-modified genes involved in the jasmonic acid signaling and phenylpropanoid biosynthesis pathways of rice in response to Spodoptera frugiperda infestation.
Abstract
Physiological and molecular mechanisms underlying plant responses to insect herbivores have been well studied, while epigenetic modifications such as histone acetylation and their potential regulation at the genomic level of hidden genes remain largely unknown. Histone 3 lysine 9 acetylation (H3K9ac) is an epigenetic marker widely distributed in plants that can activate gene transcription. In this study, we provided the genome-wide profiles of H3K9ac in rice (Oryza sativa) infested by fall armyworm (Spodoptera frugiperda, FAW) using CUT&Tag-seq and RNA-seq. There were 3269 and 4609 up-regulated genes identified in plants infested by FAW larvae for 3 h and 12 h, respectively, which were mainly enriched in alpha-linolenic acid and phenylpropanoid pathways according to transcriptomic analysis. In addition, CUT&Tag-seq analysis revealed increased H3K9ac in FAW-infested plants, and there were 422 and 543 up-regulated genes enriched with H3K9ac observed at 3 h and 12 h after FAW feeding, respectively. Genes with increased H3K9ac were mainly enriched in the transcription start site (TSS), suggesting that H3K9ac is related to gene transcription. Integrative analysis of both RNA-seq and CUT&Tag-seq data showed that up-expressed genes with H3K9ac enrichment were mainly involved in the jasmonic acid (JA) and phenylpropanoid pathways. Particularly, two spermidine hydroxycinnamoyl transferase genes SHT1 and SHT2 involved in phenolamide biosynthesis were highly modified by H3K9ac in FAW-infested plants. Furthermore, the Ossht1 and Ossht2 transgenic lines exhibited decreased resistance against FAW larvae. Our findings suggest that rice responds to insect herbivory via H3K9ac epigenetic regulation in the JA signaling and phenolamide biosynthesis pathways.
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Data availability
RNA-seq and CUT&Tag-seq raw data are available from the Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) under PRJNA967581 (accession number: SAMN34598762-SAMN34598770) and the Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo) under GSE232269 (accession number: GSM7324798-GSM7324803). All data supporting the findings of this study are available from the corresponding authors on request.
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Acknowledgements
We thank Yueqin Zheng (Fujian Academy of Agricultural Sciences) and Hao Zhang (Fujian Agriculture and Forestry Univeristy) for experimental assistance and discussion. We also appreciate comments by anonymous reviewers to help improve our manuscript.
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This research was funded by the National Natural Science Foundation of China (32171512 and 31701855), Natural Science Foundation of Fujian Province (2022J01130 and 2020J02030), China Postdoctoral Science Foundation Fellowship (2019M652237 and 2020T130099), and the Science and Technology Innovation Special foundation of Fujian Agriculture and Forestry University (KFb22004XA).
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JW, RX, and YS designed the experiments. RX, RG, QL, TL, ZW, NG, FW, and LT collected samples, performed the experiments and analyzed the data. JW, RX, RS and YS wrote and revised the paper. All authors read and approved the manuscript.
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Xue, R., Guo, R., Li, Q. et al. Rice responds to Spodoptera frugiperda infestation via epigenetic regulation of H3K9ac in the jasmonic acid signaling and phenylpropanoid biosynthesis pathways. Plant Cell Rep 43, 78 (2024). https://doi.org/10.1007/s00299-024-03160-8
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DOI: https://doi.org/10.1007/s00299-024-03160-8