PRC2 Represses Hormone-Induced Somatic Embryogenesis in Vegetative Tissue of Arabidopsis thaliana
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Abstract:
Many plant cells can be reprogrammed into a pluripotent state that allows ectopic organ development. Inducing totipotent states to stimulate somatic embryo (SE) development is, however, challenging due to insufficient understanding of molecular barriers that prevent somatic cell dedifferentiation. Here we show that Polycomb repressive complex 2 (PRC2)-activity imposes a barrier to hormone-mediated transcriptional reprogramming towards somatic embryogenesis in vegetative tissue of Arabidopsis thaliana. We identify factors that enable SE development in PRC2-depleted shoot and root tissue and demonstrate that the establishment of embryogenic potential is marked by ectopic co-activation of crucial developmental regulators that specify shoot, root and embryo identity. Using inducible activation of PRC2 in PRC2-depleted cells, we demonstrate that transient reduction of PRC2 activity is sufficient for SE formation. We suggest that modulation of PRC2 activity in plant vegetative tissue combined with targeted activation of developmental pathways will open possibilities for novel approaches to cell reprogramming.Keywords:
Reprogramming
PRC2
Totipotent
Ectopic expression
The differentiated state of a somatic nucleus can be reversed to an undifferentiated stem cell with pluripotent state or a reconstructed zygote with totipotent state,which is defined as somatic reprogramming.Adult cells can be successfully reprogrammed into pluripotent stem cells in various ways,including nuclear transfer(NT),cellular fusion,culture-induced reprogramming and induced pluripotent stem cell(iPS) by expression of transcription factors in somatic cells,in which,NT and iPS techniques offer tremendous promise for future development of patient-specific therapy.However,the reprogramming efficiency of NT and iPS are still low and the mechanisms remain elusive.The future challenge will be to reveal the molecular mechanisms potentially underlying reprogramming of somatic cell using NT and iPS techniques together.
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Somatic embryogenesis is a developmental process where a plant somatic cell can dedifferentiate to a totipotent embryonic stem cell that has the ability to give rise to an embryo under appropriate conditions. This new embryo can further develop into a whole plant. In woody plants, somatic embryogenesis plays a critical role in clonal propagation and is a powerful tool for synthetic seed production, germplasm conservation, and cryopreservation. A key step in somatic embryogenesis is the transition of cell fate from a somatic cell to embryo cell. Although somatic embryogenesis has already been widely used in a number of woody species, propagating adult woody plants remains difficult. In this review, we focus on molecular mechanisms of somatic embryogenesis and its practical applications in economic woody plants. Furthermore, we propose a strategy to improve the process of somatic embryogenesis using molecular means.
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Somatic cell reprogramming (SCR) is the conversion of differentiated somatic cells into totipotent or pluripotent cells through a variety of methods. Somatic cell reprogramming also provides a platform to investigate the role of chromatin-based factors in establishing and maintaining totipotency or pluripotency, since high expression of totipotency- or pluripotency-related genes usually require an active chromatin state. Several studies in plants or mammals have recently shed light on the molecular mechanisms by which epigenetic modifications regulate the expression of totipotency or pluripotency genes by altering their chromatin states. In this review, we present a comprehensive overview of the dynamic changes in epigenetic modifications and chromatin states during reprogramming from somatic cells to totipotent or pluripotent cells. In addition, we illustrate the potential role of DNA methylation, histone modifications, histone variants, and chromatin remodeling during somatic cell reprogramming, which will pave the way to developing reliable strategies for efficient cellular reprogramming.
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Somatic cell nuclear transfer and iPS are both forms of radical cell reprogramming able to transform a fully differentiated cell type into a totipotent or pluripotent cell. Both processes, however, are hampered by low efficiency and, in the case of iPS, the application to livestock species is uncertain. Epigenetic manipulation has recently emerged as an efficient and robust alternative method for cell reprogramming. It is based upon the use of small molecules that are able to modify the levels of DNA methylation with 5-azacitidyne as one of the most widely used. Among a number of advantages, it includes the fact that it can be applied to domestic species including pig, dog and cat. Treated cells undergo a widespread demethylation which is followed by a renewed methylation pattern induced by specific chemical stimuli that lead to the desired phenotype. A detailed study of the mechanisms of epigenetic manipulation revealed that cell plasticity is achieved through the combined action of a reduced DNA methyl transferase activity with an active demethylation driven by the TET protein family. Surprisingly the same combination of molecular processes leads to the transformation of fibroblasts into iPS and regulate the epigenetic changes that take place during early development and, hence, during reprogramming following SCNT. Finally, it has recently emerged that mechanic stimuli in the form of a 3D cell rearrangement can significantly enhance the efficiency of epigenetic reprogramming as well as of maintenance of pluripotency. Interestingly these mechanic stimuli act on the same mechanisms both in epigenetic cell conversion with 5-Aza-CR and in iPS. We suggest that the balanced combination of epigenetic erasing, 3D cell rearrangement and chemical induction can go a long way to obtain ad hoc cell types that can fully exploit the current exiting development brought by gene editing and animal cloning in livestock production.
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Somatic embryogenesis is a process whereby a single cell or a group of cells are induced to form totipotent embryogenic cells. Somatic embryogenesis always served as a model system for studying the molecular mechanisms underlying the embryogenic developmental process. There is an upsurge of interest in scientists to explore the molecular understanding of embryogenesis and the involvement of different genes and proteins during this developmental process. Studies have shown that somatic embryogenesis is under a stringent coordinated control of some regulatory genes among which somatic embryogenesis receptor kinase ( SERK ) gene has claimed an important role. In recent time expression of SERK gene was identified in embryogenic cultures of many higher plants indicating its positive role in embryogenic development. Studying the impact of SERK gene on somatic as well as zygotic embryogenesis shall improve the understanding of the molecular events leading to the formation of embryogenic cultures. The review highlights the correlation of SERK gene expression during somatic embryogenesis process and diverse functions of SERK gene during developmental changes in plants.
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Many Novel approaches of epigenetic reprogramming of somatic cells have been reported. However,ethical issues caused by somatic nuclear transfer have triggered the development of alternative strategies for reprogramming somatic cells. Recently,many new advances have been acquired for reprogramming somatic cells,which could reverse differentiated somatic cells to a totipotent embryonic state,such as fusion of potential stem cells with somatic cells,incubation of cells in potential cell-free extraction and introduction of defined pluripotency factors into somatic cells. The epigenetic modification in these reprogramming processes,including germ cells and early embryoes,somatic nuclear transfer and other approaches for reprogramming of somatic cells were reviewed. Studies of epigenetics will be benefit for understanding the precise mechanism and improving the efficiency of somatic nuclear reprogramming,which will be eventually applied in the basic study and practice.
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