HIGH LEVELS OF NON-CODING RNA IN TESTES - UNVEILING THE COMPLEX ROLES OF LONG NONCODING RNAs IN Y CHROMOSOME
Male gametes are selected for reproductive glands because they have a distinct pattern of development, high genomic expression, and accessibility. This is supported by the fact that, in both plants and animals, male gametogenesis is the site of high gene expression and the expression of the heterochromatic and silenced Y chromosome in other cells. These expressions are found only in a temporary access time of spermatogenesis where the genes have a landscape of numerous transposons to satellite repeats. Even though transposons and satellite repeats threaten the potential deleterious expression in the pool they also lead to genomic rearrangements and potential new gene production due to repetitive elements. And indeed, most of the evolution in multicellular organisms arises from spermatogenesis (refer to image).
Sperm development cycle (Spermatogenesis) |
Through FISH analysis of lncRNA, it was confirmed that relatively high expression of lncRNA gene expression was found in the testes and accessory glands of Drosophila, significantly higher than previously reported. The expression of lncRNA was observed to be higher in number in the post-meiotic stage of the cell where it differentiates into spermatids. Previously done sncRNA seq showed that ~160 coding genes, roughly <0.5% expressed post-meiotically. However, in contrast, ~80% of lncRNAs are found in spermatids which states these were expressed during the development stages. The research suggests that unique classes of promoters, transcription factors, or polymerases may be involved in driving these expressions and have novel roles in sperm assembly, structure, function, or TE (transposable element) management.
Using whole genome sequencing and functional analyses, it was earlier known that the Y chromosome composes a high content of TE, satellite repeats, and pseudogenes. Often these lead to the heterochromatic (chromosomes that are densely packed and transcriptionally inactive, not arranged in a line) structure of the chromosome which leads to silencing of the chromosome in all types of cells. However, it is still a mystery how these express on sperm development and progeny. As they observed the fourteen interpreted Y chromosome coding genes, six of them were found to contain extremely large introns (also known as Mega-Genes) which were satellite repeats and TEs. The effort to replicate, transcribe, and process these states that these mega genes (such as kl-5, kl-3, kl-2, Ppr-y, WDY, and ORY) have evolutionary advantages. Around 28 co-localizing lncRNA transcripts are found in mega-gene suggesting that they have a potential contribution to proper mega-gene transcription and processing. Interestingly, four lncRNAs that are present in Y-loop structures have sequences complementary to each other and Ppr-Y mega-gene which suggests that these lncRNAs can bind to each other and then interact with the Ppr-Y mega-gene through base-pair interaction. Another lncRNA that co-localizes with kl-3 has only interacted with kl-3 and not Ppr-Y. This indicates that only a particular lncRNA interacts with a mega-gene. The researchers explain that Drosophila melanogaster Y chromosome mega-genes are from autosomal genes with small introns and to form heterochromatin formation they may have formed these repetitive units. The resulting delay in the transcript may be due to the regulation of the protein which assures that they are expressed only post-meiotically. While considering X and Y chromosome interaction, lncRNAs are playing a dynamic role. Su(Ste) genes are Y chromosomes that produce sense and antisense transcripts. Previously it was understood that Ste gene, found in the X chromosome repressed by a ping-pong mechanism involving piRNAs (PIWI-interacting RNAs). However, the latest research shows that Ste gene is initiated by maternally provided TE fragments (1360/hoppel TEs) that bind to the 5’end of the Su(Ste) antisense transcripts. Their result shows that Su(Ste) sense transcripts are expressed before the expression of Ste genes which helps in transcribing sufficient piRNAs from Su(Ste) antisense transcripts. The Su(Ste) system evolved through the insertion of hoppel/1360 TEs into a Y chromosome Su(Ste) progenitor gene, leading to the creation of a new lncRNA gene (Su(Ste)-AS) that produces antisense transcripts. The amplification of these Su(Ste)/hoppel units has led to the current system that controls Ste gene expression. Moreover, several lncRNAs (Rox1, flam, Su(Ste)-AS) are found in spermatid nuclei and sperm tails, as well as in lumens of seminal vesicles, ejaculatory ducts, and accessory glands. This widespread presence suggests that these lncRNAs may play roles in sperm function and possibly influence progeny development. So researchers suggest that newly identified lncRNA-based particles hold significant potential for advancing the creation of novel RNA-based therapies. REFERENCE Shao Z, Hu J, Jandura A, et al. Spatially revealed roles for lncRNAs in Drosophila spermatogenesis, Y chromosome function and evolution. Nat Commun. 2024;15:3806. doi: 10.1038/s41467-024-47346-w. IMAGE CREDITS
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