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

Abstract

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.

The nucleoporin NUP160 and NUP96 regulate nucleocytoplasmic export of mRNAs and participate in ethylene signaling and response in Arabidopsis

“…In addition to nucleoporins, it was reported that the RNA helicase UAP56 can interacts with ALY and UIEF1/2 (UAP56-INTERACTING EXPORT FACTOR1 and 2), and participate in the regulation of mRNAs nucleocytosolic transport (Pfaff et al, 2018;Ehrnsberger et al, 2019b). Interestingly, a recent study reported that post-transcriptional splicing of mRNAs was involved in their nucleocytosolic exporting (Rudzka et al 2022). Without a doubt, more efforts are needed to study the effects of pre-mRNA splicing on its nuclear exportation in the future research.…”

Function of Cajal Bodies in Nuclear RNA Retention in A. thaliana Leaves Subjected to Hypoxia

“…Only non-fully spliced Sm protein transcripts were stored in the CBs. Retained introns are spliced at precisely defined times, and fully mature mRNAs are released into the cytoplasm, where Sm proteins are produced [ 49 ]. Our results show a slightly different pattern retention of RNA with introns in the nuclei of somatic cells.…”

“…For example, in animal cells, mRNA with introns are in nuclear speckles where the post-transcriptional process of their removal may take place [ 60 , 61 ]. In plants, non-fully spliced transcripts were detected in nuclear speckles [ 57 ] in microspores of Marsilea vestita and in CBs in Larix decidua [ 49 ]. Our results showed that RNA with introns accumulated in the nuclei devoid of CBs in leaf cells.…”

“…This indicates that the function of CBs in RNA retention in the leaves' nuclei could be different from that in the roots and may rely on regulating the quantity of transcripts in the nucleus in a way other than only the accumulation/storage of transcripts. Recently, Rudzka et al (2022) [49] showed the involvement of CBs in the retention of mRNA isoforms with introns in larix microspores. Only non-fully spliced Sm protein transcripts were stored in the CBs.…”

“…Processes involving the role of CBs in snRNP biogenesis include snRNA methylation, scaRNP-mediated pseudouridylation, and the formation of a preinitiation complex consisting of U4, U5, and U6 snRNPs [ 47 , 48 ]. It has also been demonstrated that CBs participate in mRNA storage in both somatic and generative cells [ 38 , 49 ]. The A. thaliana ncb-1 mutants devoid of CBs show a lower tolerance to hypoxia than the wild type, which might be connected to a much lower accumulation of poly(A + ) RNA in the nucleus of ncb-1 in comparison to the wild-type.…”