Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass

Ayyappan, Vasudevan; Sripathi, Venkateswara R.; Xie, Shaojun; Saha, Malay C.; Hayford, Rita; Serba, Desalegn D.; Subramani, Mayavan; Thimmapuram, Jyothi; Todd, Antonette; Kalavacharla, Venu Kal

doi:10.1186/s12864-024-10068-w

Title: Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass

Journal Article · 29 February 2024 · BMC Genomics

DOI: https://doi.org/10.1186/s12864-024-10068-w · OSTI ID:2471089

Ayyappan, Vasudevan ^[1]; Sripathi, Venkateswara R. ^[2]; Xie, Shaojun ^[3]; Saha, Malay C. ^[4]; Hayford, Rita ^[5]; Serba, Desalegn D. ^[6]; Subramani, Mayavan ^[1]; Thimmapuram, Jyothi ^[3]; Todd, Antonette ^[1]; Kalavacharla, Venu Kal ^[1]

Delaware State Univ., Dover, DE (United States)
Alabama A&M Univ., Normal, AL (United States)
Purdue Univ., West Lafayette, IN (United States)
Noble Research Institute, Ardmore, OK (United States)
Univ. of Delaware, Newark, DE (United States)
US Department of Agriculture (USDA), Maricopa, AZ (United States)

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.

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Research Organization:: USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: USDOE; National Science Foundation (NSF)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2471089

Journal Information:: BMC Genomics, Journal Name: BMC Genomics Journal Issue: 1 Vol. 25; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Elucidation of Complex Nature of PEG Induced Drought-Stress Response in Rice Root Using Comparative Proteomics Approach Agrawal, Lalit; Gupta, Swati; Mishra, Shashank K. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01466	journal	September 2016
MADS-Box Genes Are Key Components of Genetic Regulatory Networks Involved in Abiotic Stress and Plastic Developmental Responses in Plants Castelán-Muñoz, Natalia; Herrera, Joel; Cajero-Sánchez, Wendy Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00853	journal	July 2019
Lectin Receptor-Like Kinases: The Sensor and Mediator at the Plant Cell Surface Sun, Yali; Qiao, Zhenzhen; Muchero, Wellington Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.596301	journal	December 2020
Abscisic Acid-Induced Stomatal Closure: An Important Component of Plant Defense Against Abiotic and Biotic Stress Bharath, Pulimamidi; Gahir, Shashibhushan; Raghavendra, Agepati S. Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.615114	journal	March 2021
Involvement of JMJ15 in the dynamic change of genome-wide H3K4me3 in response to salt stress Shen, Yuan; Chi, Yuhao; Lu, Shun Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.1009723	journal	September 2022
Genome-wide analysis of transcriptome and histone modifications in Brassica napus hybrid Ma, Meng; Zhong, Wenying; Zhang, Qing Frontiers in Plant Science, Vol. 14 https://doi.org/10.3389/fpls.2023.1123729	journal	January 2023
Genome-Wide Identification of RNA Silencing-Related Genes and Their Expressional Analysis in Response to Heat Stress in Barley (Hordeum vulgare L.) Hamar, Éva; Szaker, Henrik Mihály; Kis, András Biomolecules, Vol. 10, Issue 6 https://doi.org/10.3390/biom10060929	journal	June 2020
Dynamics of H3K4me3 Chromatin Marks Prevails over H3K27me3 for Gene Regulation during Flower Morphogenesis in Arabidopsis thaliana Engelhorn, Julia; Blanvillain, Robert; Kröner, Christian Epigenomes, Vol. 1, Issue 2 https://doi.org/10.3390/epigenomes1020008	journal	June 2017
Genomic Features of Open Chromatin Regions (OCRs) in Wild Soybean and Their Effects on Gene Expressions Huang, Ming-Kun; Zhang, Ling; Zhou, Li-Meng Genes, Vol. 12, Issue 5 https://doi.org/10.3390/genes12050640	journal	April 2021
Basic Helix-Loop-Helix (bHLH) Transcription Factors Regulate a Wide Range of Functions in Arabidopsis Hao, Yaqi; Zong, Xiumei; Ren, Pan International Journal of Molecular Sciences, Vol. 22, Issue 13 https://doi.org/10.3390/ijms22137152	journal	July 2021
Arabidopsis LSH8 Positively Regulates ABA Signaling by Changing the Expression Pattern of ABA-Responsive Proteins Zou, Jinpeng; Li, Zhifang; Tang, Haohao International Journal of Molecular Sciences, Vol. 22, Issue 19 https://doi.org/10.3390/ijms221910314	journal	September 2021
Genome-Wide Mapping of Histone H3 Lysine 4 Trimethylation (H3K4me3) and Its Involvement in Fatty Acid Biosynthesis in Sunflower Developing Seeds Moreno-Pérez, Antonio J.; Santos-Pereira, José M.; Martins-Noguerol, Raquel Plants, Vol. 10, Issue 4 https://doi.org/10.3390/plants10040706	journal	April 2021
Reactive oxygen species generation and signaling in plants Tripathy, Baishnab Charan; Oelmüller, Ralf Plant Signaling & Behavior, Vol. 7, Issue 12 https://doi.org/10.4161/psb.22455	journal	December 2012
Allelochemicals as Growth Stimulators for Drought Stressed Maize Maqbool, Nazimah; Sadiq, Rumana American Journal of Plant Sciences, Vol. 08, Issue 05 https://doi.org/10.4236/ajps.2017.85065	journal	January 2017
Genome-wide analyses of direct target genes of four rice NAC-domain transcription factors involved in drought tolerance Chung, Pil; Jung, Harin; Choi, Yang figshare https://doi.org/10.6084/m9.figshare.c.3976329	collection	January 2018
Comparative transcriptome analysis and ChIP-sequencing reveals stage-specific gene expression and regulation profiles associated with pollen wall formation in Brassica rapa Shen, Xiuping; Xu, Liai; Liu, Yanhong figshare https://doi.org/10.6084/m9.figshare.c.4459310	collection	January 2019
Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato Zeng, Zixian; Zhang, Wenli; Marand, Alexandre figshare https://doi.org/10.6084/m9.figshare.c.4545398.v1	collection	January 2019
Global analysis of switchgrass (Panicum virgatum L.) transcriptomes in response to interactive effects of drought and heat stresses Hayford, Rita K.; Serba, Desalegn D.; Xie, Shaojun figshare https://doi.org/10.6084/m9.figshare.c.5883880.v1	collection	January 2022
SET-9 and SET-26 are H3K4me3 readers and play critical roles in germline development and longevity Wang, Wenke; Chaturbedi, Amaresh; Wang, Minghui eLife, Vol. 7 https://doi.org/10.7554/eLife.34970	journal	May 2018
S-adenosylmethionine synthases specify distinct H3K4me3 populations and gene expression patterns during heat stress Godbole, Adwait A.; Gopalan, Sneha; Nguyen, Thien-Kim eLife, Vol. 12 https://doi.org/10.7554/eLife.79511	journal	February 2023

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59 BASIC BIOLOGICAL SCIENCES
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Drought
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Title: Genome-wide profiling of histone (H3) lysine 4 (K4) tri-methylation (me3) under drought, heat, and combined stresses in switchgrass

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