Transcriptomic profiling reveals histone acetylation-regulated genes involved in somatic embryogenesis in Arabidopsis thaliana

Abstract Background Somatic embryogenesis (SE) exemplifies the unique developmental plasticity of plant cells. The regulatory processes, including epigenetic modifications controlling embryogenic reprogramming of cell transcriptome, have just started to be revealed. Results To identify the genes of histone acetylation-regulated expression in SE, we analyzed global transcriptomes of Arabidopsis explants undergoing embryogenic induction in response to treatment with histone deacetylase inhibitor, trichostatin A (TSA). The TSA-induced and auxin (2,4-dichlorophenoxyacetic acid; 2,4-D)-induced transcriptomes were compared. RNA-seq results revealed the similarities of the TSA- and auxin-induced transcriptomic responses that involve extensive deregulation, mostly repression, of the majority of genes. Within the differentially expressed genes (DEGs), we identified the master regulators (transcription factors - TFs) of SE, genes involved in biosynthesis, signaling, and polar transport of auxin and NITRILASE-encoding genes of the function in indole-3-acetic acid (IAA) biosynthesis. TSA-upregulated TF genes of essential functions in auxin-induced SE, included LEC1/LEC2 , FUS3 , AGL15 , MYB118 , PHB , PHV , PLTs , and WUS/WOXs . The TSA-induced transcriptome revealed also extensive upregulation of stress-related genes, including those related to stress hormone biosynthesis. In line with transcriptomic data, TSA-induced explants accumulated salicylic acid (SA) and abscisic acid (ABA), suggesting the role of histone acetylation (Hac) in regulating stress hormone-related responses during SE induction. Since mostly the adaxial side of cotyledon explant contributes to SE induction, we also identified organ polarity-related genes responding to TSA treatment, including AIL7/PLT7 , RGE1 , LBD18 , 40 , HB32 , CBF1 , and ULT2 . Analysis of the relevant mutants supported the role of polarity-related genes in SE induction. Conclusion The study results provide a step forward in deciphering the epigenetic network controlling embryogenic transition in somatic cells of plants.

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Journal
BMC Genomics
Published
2024-08-15
DOI
https://doi.org/10.1186/s12864-024-10623-5
Citations
10
Primary Topic
Plant Molecular Biology Research
Type
article
Field-Weighted Citation Impact
6.00

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article

Transcriptomic profiling reveals histone acetylation-regulated genes involved in somatic embryogenesis in Arabidopsis thaliana

Małgorzata D. Gaj, Mirosław Kwaśniewski, Karolina Chwiałkowska, Barbara Wójcikowska et al.
10 citations
BMC Genomics
Plant Molecular Biology Research
6.00
article

Transcriptomic profiling reveals histone acetylation-regulated genes involved in somatic embryogenesis in Arabidopsis thaliana

Małgorzata D. Gaj, Mirosław Kwaśniewski, Karolina Chwiałkowska, Barbara Wójcikowska, Agnieszka Kiwior-Wesołowska, Joanna Morończyk, Sylvie Citerne, Katarzyna Nowak, Jacek Francikowski, Anna M. Wójcik
article en
10 citations

Abstract

Abstract Background Somatic embryogenesis (SE) exemplifies the unique developmental plasticity of plant cells. The regulatory processes, including epigenetic modifications controlling embryogenic reprogramming of cell transcriptome, have just started to be revealed. Results To identify the genes of histone acetylation-regulated expression in SE, we analyzed global transcriptomes of Arabidopsis explants undergoing embryogenic induction in response to treatment with histone deacetylase inhibitor, trichostatin A (TSA). The TSA-induced and auxin (2,4-dichlorophenoxyacetic acid; 2,4-D)-induced transcriptomes were compared. RNA-seq results revealed the similarities of the TSA- and auxin-induced transcriptomic responses that involve extensive deregulation, mostly repression, of the majority of genes. Within the differentially expressed genes (DEGs), we identified the master regulators (transcription factors - TFs) of SE, genes involved in biosynthesis, signaling, and polar transport of auxin and NITRILASE-encoding genes of the function in indole-3-acetic acid (IAA) biosynthesis. TSA-upregulated TF genes of essential functions in auxin-induced SE, included LEC1/LEC2 , FUS3 , AGL15 , MYB118 , PHB , PHV , PLTs , and WUS/WOXs . The TSA-induced transcriptome revealed also extensive upregulation of stress-related genes, including those related to stress hormone biosynthesis. In line with transcriptomic data, TSA-induced explants accumulated salicylic acid (SA) and abscisic acid (ABA), suggesting the role of histone acetylation (Hac) in regulating stress hormone-related responses during SE induction. Since mostly the adaxial side of cotyledon explant contributes to SE induction, we also identified organ polarity-related genes responding to TSA treatment, including AIL7/PLT7 , RGE1 , LBD18 , 40 , HB32 , CBF1 , and ULT2 . Analysis of the relevant mutants supported the role of polarity-related genes in SE induction. Conclusion The study results provide a step forward in deciphering the epigenetic network controlling embryogenic transition in somatic cells of plants.

BMC GenomicsVol. 25(1)
Medical University of Białystok (PL), AgroParisTech (FR), Université Paris-Saclay (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Institut Jean-Pierre Bourgin (FR), University of Silesia in Katowice (PL)
Agence Nationale de la Recherche, AgroParisTech, Université Paris-Saclay, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Good health and well-being
Openalex Percentile: Top 4%
Plant Molecular Biology Research
6.00
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