Nuclear retention of pre-mRNA involving Cajal bodies during meiotic prophase in plants

Abstract

Gene regulation ensures that the appropriate genes are expressed at the proper times. Nuclear retention of incompletely spliced or mature mRNAs emerges as a novel, previously underappreciated layer of post-transcriptional gene regulation. Studies on this phenomenon indicated that it exerted significant impact on the regulation of gene expression by regulating export and translation delay, which allows synthesis of specific proteins in response to a stimulus, e.g. under stress conditions or at strictly controlled time points, e.g. during cell differentiation or development. Here, we found that transcription in microsporocytes, during prophase of the first meiotic division, occurs in pulsatile manner. After each pulse, the transcriptional activity is silenced, but the transcripts synthesized at this time are not exported immediately to the cytoplasm, but are retained in the nucleoplasm and Cajal bodies (CBs). In contrast to nucleoplasm, mature transcripts were not found in CBs. Only non-fully-spliced transcripts with retained introns were stored in the CBs. Retained introns are spliced at precisely defined times, and fully mature mRNAs are released into the cytoplasm, where the proteins are produced. These proteins are necessary for further cell development during meiotic prophase. Our findings provide new insight into the regulatory mechanisms of gene expression based on mRNA retention in the nucleus during the development of generative cells in plants. Similar processes were observed during spermatogenesis in animals. This indicates the existence of an evolutionarily conserved mechanism of gene expression regulation during generative cells development in Eukaryota.

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

“…The role of mRNAs retention in the cell nucleus in the process of post-transcriptional reduction of transcriptional noise was discovered in the last decade and is now extensively studied. It appears to be common in all eukaryotes, both unicellular, such as yeasts [11] and multicellular plants [12,13] as well as animals [14].…”

“…Recent studies suggested another role of nuclear mRNAs retention, namely strict temporal control of specific mRNAs export to cytoplasm [11][12][13][14]. Furthermore, regulation of gene expression by nuclear mRNA retention occurs in mammalian metabolic tissues both under stress [15,16] and normal physiological conditions [14].…”

“…Furthermore, regulation of gene expression by nuclear mRNA retention occurs in mammalian metabolic tissues both under stress [15,16] and normal physiological conditions [14]. It was also found in generative cells that require the expression of specific proteins at a time strictly defined by their developmental stage [11][12][13]. Retained transcripts are localized in the nucleoplasm, nuclear basket, and nuclear domains such as nuclear speckles, paraspeckles, Cajal bodies, and nuclear foci ("dots") [13,[17][18][19][20].…”

“…It was also found in generative cells that require the expression of specific proteins at a time strictly defined by their developmental stage [11][12][13]. Retained transcripts are localized in the nucleoplasm, nuclear basket, and nuclear domains such as nuclear speckles, paraspeckles, Cajal bodies, and nuclear foci ("dots") [13,[17][18][19][20]. mRNA retention may be due to an unspliced intron, a poly(A) tail with an altered length, cis-elements, or convert adenosine to inosine [13,[17][18][19][20].…”

“…Retained transcripts are localized in the nucleoplasm, nuclear basket, and nuclear domains such as nuclear speckles, paraspeckles, Cajal bodies, and nuclear foci ("dots") [13,[17][18][19][20]. mRNA retention may be due to an unspliced intron, a poly(A) tail with an altered length, cis-elements, or convert adenosine to inosine [13,[17][18][19][20]. Transcripts accumulated in nuclear foci in S. cerevisiae have a hippo-or hyperacetylated poly(A) tail [19].…”