Unusual RNA polymerase II patterns in meiotic prophase I in Nannospalax xanthodon: insights into chromatin, telomeres, and sex chromosomes

Background: Meiotic transcription is a highly regulated process involving stage-specific chromatin remodeling and dynamic RNA polymerase II (RNAPII) activity. Nevertheless, our current understanding is largely based on classical model organisms, while many nonmodel mammals remain unexplored. This study investigates the transcriptional dynamics and chromatin features during meiotic prophase I in Nannospalax xanthodon, a subterranean blind mole rat species with extensive intraspecific karyotype variation.Materials and methods: Using immunofluorescence, we analyzed synapsis and transcriptional activity in spermatocyte nuclei of two geographically distant N. xanthodon males, detecting SYCP3, CREST, γH2AFX, and phosphorylated RNAPII (Ser5, Ser2). Telomereassociated proteins RAP1 and TERT were also examined to assess transcriptional activity at chromosomal ends.Results: Transcriptional activity was detected at all substages of prophase I. Unlike classical models, N. xanthodon exhibited no sharp pachytene-specific transcriptional reactivation; instead, RNAPII-Ser2 and Ser5 signals increased gradually from leptotene to pachytene. Notably, RNAPII-Ser5, but not Ser2, was consistently localized at telomeric regions of autosomes and sex chromosomes. These RNAPIISer5 foci coincided with RAP1-positive telomeres, suggesting a poised but transcriptionally inactive polymerase state at chromosome ends. The variability of RNAPII signals around the XY bivalent may also suggest a dynamic regulation of sex chromosome silencing. This is the first analysis of meiotic transcription in mole rats. The gradual transcriptional enhancement in the chromatin of prophase I nuclei and the RNAPII-Ser5 enrichment at telomeres reflect species-specific regulatory features.Conclusions: These findings highlight the importance of investigating nonmodel organisms to uncover novel mechanisms of meiotic regulation and suggest that transcriptional control during meiosis may be more evolutionarily diverse than previously recognized.