Different Patterns of mRNA Nuclear Retention during Meiotic Prophase in Larch Microsporocytes

Majewska, Karolina; Wróblewska-Ankiewicz, Patrycja; Rudzka, Magda; Hyjek-Składanowska, Malwina; Gołębiewski, Marcin; Smoliński, Dariusz Jan; Kołowerzo-Lubnau, Agnieszka

doi:10.3390/ijms22168501

Cited by 3 publications

(1 citation statement)

References 37 publications

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“…Accordingly, several reports have demonstrated that mRNA nuclear retention due to retained introns can also be used as a mechanism for the temporal control of gene expression. Certain introns were found to be post-transcriptionally removed at distinct times, allowing regulated mRNA export and translation, which is especially relevant during cell differentiation [23][24][25].…”

Section: Quality Control Of Splicing In the Nucleus-retention Or Export Of Mrnamentioning

confidence: 99%

Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1

Krebber

2021

IJMS

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Pre-mRNA splicing is critical for cells, as defects in this process can lead to altered open reading frames and defective proteins, potentially causing neurodegenerative diseases and cancer. Introns are removed in the nucleus and splicing is documented by the addition of exon-junction-complexes (EJCs) at exon-exon boundaries. This “memory” of splicing events is important for the ribosome, which translates the RNAs in the cytoplasm. In case a stop codon was detected before an EJC, translation is blocked and the RNA is eliminated by the nonsense-mediated decay (NMD). In the model organism Saccharomyces cerevisiae, two guard proteins, Gbp2 and Hrb1, have been identified as nuclear quality control factors for splicing. In their absence, intron-containing mRNAs leak into the cytoplasm. Their presence retains transcripts until the process is completed and they release the mRNAs by recruitment of the export factor Mex67. On transcripts that experience splicing problems, these guard proteins recruit the nuclear RNA degradation machinery. Interestingly, they continue their quality control function on exported transcripts. They support NMD by inhibiting translation and recruiting the cytoplasmic degradation factors. In this way, they link the nuclear and cytoplasmic quality control systems. These discoveries are also intriguing for humans, as homologues of these guard proteins are present also in multicellular organisms. Here, we provide an overview of the quality control mechanisms of pre-mRNA splicing, and present Gbp2 and Hrb1, as well as their human counterparts, as important players in these pathways.

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Section: Quality Control Of Splicing In the Nucleus-retention Or Export Of Mrnamentioning

confidence: 99%

Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1

Krebber

2021

IJMS

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Functional nuclear retention of pre-mRNA involving Cajal bodies during meiotic prophase in European larch (Larix decidua)

et al. 2022

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Gene regulation ensures that the appropriate genes are expressed at the proper time. Nuclear retention of incompletely spliced or mature mRNAs is emerging as a novel, previously underappreciated layer of post-transcriptional regulation. Studies on this phenomenon indicated that it exerts a significant influence on the regulation of gene expression by regulating export and translation delay, which allows the synthesis of specific proteins in response to a stimulus or at strictly controlled time points, e.g. during cell differentiation or development. Here, we show that transcription in microsporocytes of European larch (Larix decidua) occurs in a pulsatile manner during prophase of the first meiotic division. Transcriptional activity was then silenced after each pulse. However, the transcripts synthesized were not exported immediately to the cytoplasm but were retained in the nucleoplasm and Cajal bodies (CBs). In contrast to the nucleoplasm, we did not detect mature transcripts in CBs, which only stored non-fully-spliced transcripts with retained introns. Notably, the retained introns were spliced at precisely defined times, and fully mature mRNAs were released into the cytoplasm for translation. As similar processes have been observed during spermatogenesis in animals, our results illustrate an evolutionarily conserved mechanism of gene expression regulation during generative cells development in Eukaryota.

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Cajal bodies: Evolutionarily conserved nuclear biomolecular condensates with properties unique to plants

et al. 2023

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Proper orchestration of the thousands of biochemical processes that are essential to the life of every cell requires highly organized cellular compartmentalization of dedicated microenvironments. There are two ways to create this intracellular segregation to optimize cellular function. One way is to create specific organelles, enclosed spaces bounded by lipid membranes that regulate macromolecular flux in and out of the compartment. A second way is via membrane-less biomolecular condensates that form due to to liquid-liquid phase separation. Although research on these membrane-less condensates has historically been performed using animal and fungal systems, recent studies have explored basic principles governing the assembly, properties, and functions of membrane-less compartments in plants. In this review, we discuss how phase separation is involved in a variety of key processes occurring in Cajal bodies (CBs), a type of biomolecular condensates found in nuclei. These processes include RNA metabolism, formation of ribonucleoproteins involved in transcription, RNA splicing, ribosome biogenesis, and telomere maintenance. Besides these primary roles of CBs, we discuss unique plant-specific functions of CBs in RNA-based regulatory pathways such as nonsense-mediated mRNA decay, mRNA retention and RNA silencing. Finally, we summarize recent progress and discuss the functions of CBs in responses to pathogen attacks and abiotic stresses, responses that may be regulated via mechanisms governed by polyADP-ribosylation. Thus, plant CBs are emerging as highly complex and multifunctional biomolecular condensates that are involved in a surprisingly diverse range of molecular mechanisms that we are just beginning to appreciate.

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Different Patterns of mRNA Nuclear Retention during Meiotic Prophase in Larch Microsporocytes

Cited by 3 publications

References 37 publications

Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1

Nuclear mRNA Quality Control and Cytoplasmic NMD Are Linked by the Guard Proteins Gbp2 and Hrb1

Functional nuclear retention of pre-mRNA involving Cajal bodies during meiotic prophase in European larch (Larix decidua)

Cajal bodies: Evolutionarily conserved nuclear biomolecular condensates with properties unique to plants

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