Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass
Abstract Background Switchgrass (Panicum virgatum L.) is a warm-season perennial (C4) grass identified as an important biofuel crop in the United States. It is well adapted to the marginal environment where heat and moisture stresses predominantly affect crop growth. However, the underlying molecula...
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| Format: | Article |
| Language: | English |
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BMC
2024-02-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-024-10068-w |
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| author | Vasudevan Ayyappan Venkateswara R. Sripathi Shaojun Xie Malay C. Saha Rita Hayford Desalegn D. Serba Mayavan Subramani Jyothi Thimmapuram Antonette Todd Venu Kal Kalavacharla |
| author_facet | Vasudevan Ayyappan Venkateswara R. Sripathi Shaojun Xie Malay C. Saha Rita Hayford Desalegn D. Serba Mayavan Subramani Jyothi Thimmapuram Antonette Todd Venu Kal Kalavacharla |
| author_sort | Vasudevan Ayyappan |
| collection | DOAJ |
| description | Abstract Background Switchgrass (Panicum virgatum L.) is a warm-season perennial (C4) grass identified as an important biofuel crop in the United States. It is well adapted to the marginal environment where heat and moisture stresses predominantly affect crop growth. However, the underlying molecular mechanisms associated with heat and drought stress tolerance still need to be fully understood in switchgrass. The methylation of H3K4 is often associated with transcriptional activation of genes, including stress-responsive. Therefore, this study aimed to analyze genome-wide histone H3K4-tri-methylation in switchgrass under heat, drought, and combined stress. Results In total, ~ 1.3 million H3K4me3 peaks were identified in this study using SICER. Among them, 7,342; 6,510; and 8,536 peaks responded under drought (DT), drought and heat (DTHT), and heat (HT) stresses, respectively. Most DT and DTHT peaks spanned 0 to + 2000 bases from the transcription start site [TSS]. By comparing differentially marked peaks with RNA-Seq data, we identified peaks associated with genes: 155 DT-responsive peaks with 118 DT-responsive genes, 121 DTHT-responsive peaks with 110 DTHT-responsive genes, and 175 HT-responsive peaks with 136 HT-responsive genes. We have identified various transcription factors involved in DT, DTHT, and HT stresses. Gene Ontology analysis using the AgriGO revealed that most genes belonged to biological processes. Most annotated peaks belonged to metabolite interconversion, RNA metabolism, transporter, protein modifying, defense/immunity, membrane traffic protein, transmembrane signal receptor, and transcriptional regulator protein families. Further, we identified significant peaks associated with TFs, hormones, signaling, fatty acid and carbohydrate metabolism, and secondary metabolites. qRT-PCR analysis revealed the relative expressions of six abiotic stress-responsive genes (transketolase, chromatin remodeling factor-CDH3, fatty-acid desaturase A, transmembrane protein 14C, beta-amylase 1, and integrase-type DNA binding protein genes) that were significantly (P < 0.05) marked during drought, heat, and combined stresses by comparing stress-induced against un-stressed and input controls. Conclusion Our study provides a comprehensive and reproducible epigenomic analysis of drought, heat, and combined stress responses in switchgrass. Significant enrichment of H3K4me3 peaks downstream of the TSS of protein-coding genes was observed. In addition, the cost-effective experimental design, modified ChIP-Seq approach, and analyses presented here can serve as a prototype for other non-model plant species for conducting stress studies. |
| first_indexed | 2024-03-07T15:19:30Z |
| format | Article |
| id | doaj.art-efaed5db28a3437e93d056b85a3e2e47 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-03-07T15:19:30Z |
| publishDate | 2024-02-01 |
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| series | BMC Genomics |
| spelling | doaj.art-efaed5db28a3437e93d056b85a3e2e472024-03-05T17:47:07ZengBMCBMC Genomics1471-21642024-02-0125111910.1186/s12864-024-10068-wGenome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrassVasudevan Ayyappan0Venkateswara R. Sripathi1Shaojun Xie2Malay C. Saha3Rita Hayford4Desalegn D. Serba5Mayavan Subramani6Jyothi Thimmapuram7Antonette Todd8Venu Kal Kalavacharla9Molecular Genetics and Epigenomics Laboratory, Delaware State UniversityCenter for Molecular Biology, Alabama A&M UniversityBioinformatics Core, Purdue UniversityNoble Research Institute, LLCCenter for Bioinformatics and Computational Biology, University of DelawareUSDA-ARS, U.S. Arid Land Agricultural Research CenterMolecular Genetics and Epigenomics Laboratory, Delaware State UniversityBioinformatics Core, Purdue UniversityMolecular Genetics and Epigenomics Laboratory, Delaware State UniversityMolecular Genetics and Epigenomics Laboratory, Delaware State UniversityAbstract Background Switchgrass (Panicum virgatum L.) is a warm-season perennial (C4) grass identified as an important biofuel crop in the United States. It is well adapted to the marginal environment where heat and moisture stresses predominantly affect crop growth. However, the underlying molecular mechanisms associated with heat and drought stress tolerance still need to be fully understood in switchgrass. The methylation of H3K4 is often associated with transcriptional activation of genes, including stress-responsive. Therefore, this study aimed to analyze genome-wide histone H3K4-tri-methylation in switchgrass under heat, drought, and combined stress. Results In total, ~ 1.3 million H3K4me3 peaks were identified in this study using SICER. Among them, 7,342; 6,510; and 8,536 peaks responded under drought (DT), drought and heat (DTHT), and heat (HT) stresses, respectively. Most DT and DTHT peaks spanned 0 to + 2000 bases from the transcription start site [TSS]. By comparing differentially marked peaks with RNA-Seq data, we identified peaks associated with genes: 155 DT-responsive peaks with 118 DT-responsive genes, 121 DTHT-responsive peaks with 110 DTHT-responsive genes, and 175 HT-responsive peaks with 136 HT-responsive genes. We have identified various transcription factors involved in DT, DTHT, and HT stresses. Gene Ontology analysis using the AgriGO revealed that most genes belonged to biological processes. Most annotated peaks belonged to metabolite interconversion, RNA metabolism, transporter, protein modifying, defense/immunity, membrane traffic protein, transmembrane signal receptor, and transcriptional regulator protein families. Further, we identified significant peaks associated with TFs, hormones, signaling, fatty acid and carbohydrate metabolism, and secondary metabolites. qRT-PCR analysis revealed the relative expressions of six abiotic stress-responsive genes (transketolase, chromatin remodeling factor-CDH3, fatty-acid desaturase A, transmembrane protein 14C, beta-amylase 1, and integrase-type DNA binding protein genes) that were significantly (P < 0.05) marked during drought, heat, and combined stresses by comparing stress-induced against un-stressed and input controls. Conclusion Our study provides a comprehensive and reproducible epigenomic analysis of drought, heat, and combined stress responses in switchgrass. Significant enrichment of H3K4me3 peaks downstream of the TSS of protein-coding genes was observed. In addition, the cost-effective experimental design, modified ChIP-Seq approach, and analyses presented here can serve as a prototype for other non-model plant species for conducting stress studies.https://doi.org/10.1186/s12864-024-10068-wSwitchgrassDroughtHeatStressChromatinChIP-Seq |
| spellingShingle | Vasudevan Ayyappan Venkateswara R. Sripathi Shaojun Xie Malay C. Saha Rita Hayford Desalegn D. Serba Mayavan Subramani Jyothi Thimmapuram Antonette Todd Venu Kal Kalavacharla Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass BMC Genomics Switchgrass Drought Heat Stress Chromatin ChIP-Seq |
| title | Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass |
| title_full | Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass |
| title_fullStr | Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass |
| title_full_unstemmed | Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass |
| title_short | Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass |
| title_sort | genome wide profiling of histone h3 lysine 4 k4 tri methylation me3 under drought heat and combined stresses in switchgrass |
| topic | Switchgrass Drought Heat Stress Chromatin ChIP-Seq |
| url | https://doi.org/10.1186/s12864-024-10068-w |
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