AGL15 Controls the Embryogenic Reprogramming of Somatic Cells in Arabidopsis through the Histone Acetylation-Mediated Repression of the miRNA Biogenesis Genes

Nowak, Katarzyna; Morończyk, Joanna; Wójcik, Anna; Gaj, Małgorzata D.

doi:10.3390/ijms21186733

Cited by 17 publications

(21 citation statements)

References 101 publications

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“…Finally, it is important to mention a recent study in Arabidopsis [ 68 ] showing that the control of miRNA pathways can be mediated by histone acetylation during the embryogenic reprogramming. This involved the transcription factor AGAMOUS-LIKE 15 (AGL15), which is capable of regulating miR156 both by transcriptional activation of MIR156 or containment of its levels through repression of the miRNA biogenesis genes DCL1 , SERRATE and HEN1 .…”

Section: Induction and Early Somatic Embryogenesismentioning

confidence: 99%

“…This involved the transcription factor AGAMOUS-LIKE 15 (AGL15), which is capable of regulating miR156 both by transcriptional activation of MIR156 or containment of its levels through repression of the miRNA biogenesis genes DCL1 , SERRATE and HEN1 . In experiments involving the use of an inhibitor of the HDAC histone deacetylases, the authors showed that histone deacetylation is associated with the repression of miRNA processing, and this is mediated by AGL15 [ 68 ].…”

Section: Induction and Early Somatic Embryogenesismentioning

confidence: 99%

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Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

Alves

Cordeiro

Correia

et al. 2021

Plants

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Small non-coding RNAs (sncRNAs) are molecules with important regulatory functions during development and environmental responses across all groups of terrestrial plants. In seed plants, the development of a mature embryo from the zygote follows a synchronized cell division sequence, and growth and differentiation events regulated by highly regulated gene expression. However, given the distinct features of the initial stages of embryogenesis in gymnosperms and angiosperms, it is relevant to investigate to what extent such differences emerge from differential regulation mediated by sncRNAs. Within these, the microRNAs (miRNAs) are the best characterized class, and while many miRNAs are conserved and significantly represented across angiosperms and other seed plants during embryogenesis, some miRNA families are specific to some plant lineages. Being a model to study zygotic embryogenesis and a relevant biotechnological tool, we systematized the current knowledge on the presence and characterization of miRNAs in somatic embryogenesis (SE) of seed plants, pinpointing the miRNAs that have been reported to be associated with SE in angiosperm and gymnosperm species. We start by conducting an overview of sncRNA expression profiles in the embryonic tissues of seed plants. We then highlight the miRNAs described as being involved in the different stages of the SE process, from its induction to the full maturation of the somatic embryos, adding references to zygotic embryogenesis when relevant, as a contribution towards a better understanding of miRNA-mediated regulation of SE.

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Section: Induction and Early Somatic Embryogenesismentioning

confidence: 99%

Section: Induction and Early Somatic Embryogenesismentioning

confidence: 99%

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

Alves

Cordeiro

Correia

et al. 2021

Plants

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“…The ChIP method of Yelagandula et al [ 78 ] with some modifications that were described by Nowak et al [ 71 ] was used. Chromatin was extracted from the cultured explants (~50 mg of tissue) that had been treated with 1% formaldehyde for 20 min on ice under a vacuum.…”

Section: Methodsmentioning

confidence: 99%

“…A LightCycler 480 (Roche, Basel, Switzerland) real-time detection system was used to analyze the relative acetylation level of the WUS -gene-associated chromatin. The qPCR reaction was conducted according to Nowak et al [ 71 ]. The primers that were used in the qPCR were designed using Primer3Plus software (version 3, Molbi, Michelstand, Germany).…”

Section: Methodsmentioning

confidence: 99%

“…HDA6 and HDA19 redundantly control the repression of an embryo-specific gene function, and the repression of the HDA6/19 function results in a spontaneous somatic-embryo development in germinating seedlings [ 66 ], thereby suggesting the role of these HDACs during SE control. Recently, the cooperation of HDA6/HDA19 with the AGL15 and the TOPLESS co-repressors of the SIN3/HDAC (SWI-INDEPENDENT 3/HISTONE DEACETYLASE) silencing complex was revealed to control the miRNA biogenesis genes in SE induction [ 71 ].…”

Section: Introductionmentioning

confidence: 99%

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miR172 Regulates WUS during Somatic Embryogenesis in Arabidopsis via AP2

Nowak

Morończyk

Grzyb

et al. 2022

Cells

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In plants, the embryogenic transition of somatic cells requires the reprogramming of the cell transcriptome, which is under the control of genetic and epigenetic factors. Correspondingly, the extensive modulation of genes encoding transcription factors and miRNAs has been indicated as controlling the induction of somatic embryogenesis in Arabidopsis and other plants. Among the MIRNAs that have a differential expression during somatic embryogenesis, members of the MIRNA172 gene family have been identified, which implies a role of miR172 in controlling the embryogenic transition in Arabidopsis. In the present study, we found a disturbed expression of both MIRNA172 and candidate miR172-target genes, including AP2, TOE1, TOE2, TOE3, SMZ and SNZ, that negatively affected the embryogenic response of transgenic explants. Next, we examined the role of AP2 in the miR172-mediated mechanism that controls the embryogenic response. We found some evidence that by controlling AP2, miR172 might repress the WUS that has an important function in embryogenic induction. We showed that the mechanism of the miR172-AP2-controlled repression of WUS involves histone acetylation. We observed the upregulation of the WUS transcripts in an embryogenic culture that was overexpressing AP2 and treated with trichostatin A (TSA), which is an inhibitor of HDAC histone deacetylases. The increased expression of the WUS gene in the embryogenic culture of the hdac mutants further confirmed the role of histone acetylation in WUS control during somatic embryogenesis. A chromatin-immunoprecipitation analysis provided evidence about the contribution of HDA6/19-mediated histone deacetylation to AP2-controlled WUS repression during embryogenic induction. The upstream regulatory elements of the miR172-AP2-WUS pathway might involve the miR156-controlled SPL9/SPL10, which control the level of mature miR172 in an embryogenic culture.

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Understanding the evolution of miRNA biogenesis machinery in plants with special focus on rice

Chithung

Kansal

Jajo

et al. 2023

Funct Integr Genomics

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miRNA biogenesis process is an intricate and complex event consisting of many proteins working in a highly coordinated fashion. Most of these proteins have been studied in Arabidopsis; however, their orthologs and functions have not been explored in other plant species. In the present study, we have manually curated all the experimentally verified information present in the literature regarding these proteins and found a total of 98 genes involved in miRNA biogenesis in Arabidopsis. The conservation pattern of these proteins was identified in other plant species ranging from dicots to lower organisms, and we found that a major proportion of proteins involved in the pri-miRNA processing are conserved. However, nearly 20% of the genes, mostly involved in either transcription or functioning of the miRNAs, were absent in the lower organisms. Further, we manually curated a regulatory network of the core components of the biogenesis process and found that nearly half (46%) of the proteins interact with them, indicating that the processing step is perhaps the most under surveillance/regulation. We have subsequently attempted to characterize the orthologs identified in Oryza sativa, on the basis of transcriptome and epigenetic modifications under field drought conditions in order to assess the impact of drought on the process. We found several participating genes to be differentially expressed and/or epigenetically methylated under drought, although the core components like DCL1, SE, and HYL1 remain unaffected by the stress itself. The study enhances our present understanding of the biogenesis process and its regulation.

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AGL15 Controls the Embryogenic Reprogramming of Somatic Cells in Arabidopsis through the Histone Acetylation-Mediated Repression of the miRNA Biogenesis Genes

Cited by 17 publications

References 101 publications

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

Small Non-Coding RNAs at the Crossroads of Regulatory Pathways Controlling Somatic Embryogenesis in Seed Plants

miR172 Regulates WUS during Somatic Embryogenesis in Arabidopsis via AP2

Understanding the evolution of miRNA biogenesis machinery in plants with special focus on rice

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