Comparison of Y-chromosome-linked TSPY, TSPY2, and PRAMEY genes in Taurus cattle, yaks, and interspecific hybrid bulls

Abstract

Domestic yaks (Bos grunniens) and domestic Taurus cattle (Bos taurus) are closely related. An interesting phenomenon in interspecific crossings is male sterility in the F 1 hybrid (yattle) and F 2 backcross, with no late meiotic cells or spermatids in the seminiferous tubules. The mammalian Y chromosome is crucial for spermatogenesis and male fertility. This study investigated the copy number variations and mRNA of Y-transitional region genes TSPY2 (testis specific protein, Y-linked 2 and testis-specific Y-encoded protein 3-like) and PRAMEY (preferentially expressed antigen in melanoma, Y-linked), and Y-ampliconic region genes TSPY (testis-specific Y-encoded protein 1-like), ZNF280BY (zinc finger protein 280B, Y-linked) and HSFY (heatshock transcription factor, Y-linked) in mature testes from Taurus cattle, yaks, and yattle. Phylogenetic trees divided 33 copies of TSPY into major 2 types (TSPY-T1 and TSPY-T2), 19 copies of TSPY2 into 2 types (TSPY2-T1 and T2), and 8 copies of PRAMEY into 4 types (PRAMEY-T1 to T4). Searching by the Basic Local Alignment Search Tool of the TSPY2 coding sequences in GenBank revealed that TSPY2 was conserved in Bovidae. The TSPY2-T2 sequences were absent, whereas PRAMEY-T2 and PRAMEY-T4 were amplified on the yak Y chromosome. The average copy numbers of TSPY-T2 and ZNF280BY were significantly different between cattle and yaks. The TSPY-T2, TSPY2, PRAMEY, ZNF280BY, and HSFY genes were uniquely or predominantly expressed in testes. Reversetranscription quantitative PCR showed that the TSPY-T2, PRAMEY-T2, HSFY, ZNF280BY, protamine 1 (PRM1), and protamine 2 (PRM2) genes were almost not expressed in yattle. The PRM1 and PRM2 genes are used as positive markers for spermatozoa. Thus, our results showed that the genomic structure of the Ytransitional and Y-ampliconic region differed between Taurus cattle and yaks. Dysregulated expression of Yampliconic region genes TSPY-T2, HSPY, ZNF280BY, and Y-transitional region gene PRAMEY-T2 may be associated with hybrid male sterility in yattle.

Promoter hypermethylation of PIWI/piRNA pathway genes associated with diminished pachytene piRNA production in bovine hybrid male sterility

“…Indeed, promoter and CGI hypermethylation associated with silencing PIWI/piRNA pathway genes PIWIL1, DDX4, PLD6, MAEL, FKBP6, RNF17, MOV10L1, TDRD1, TDRD5, and TDRD9 (Figure 2(c)), resulted in diminished production of pachytene piRNAs in yattle testes (Figures 3(d) and 4(e). This molecular connection with histologic observations of seminiferous tubules indicated that male infertility of yattle may be due to meiosis arrest at about the pachytene stage [7]. In contrast, PIWIL2, PIWIL4, EXD1, TDRD12 are involved in prepachytene piRNA production [65][66][67][68].…”

“…F1 hybrid yattle and F2 backcross males are sterile while females are fertile. Seminiferous tubules of yattle contain few primary spermatocytes at the leptotene to pachytene stage and no spermatocytes beyond this stage [5][6][7]. Thus, the male infertility of yattle may be due to arrest of meiosis at about the pachytene stage [7].…”

“…Seminiferous tubules of yattle contain few primary spermatocytes at the leptotene to pachytene stage and no spermatocytes beyond this stage [5][6][7]. Thus, the male infertility of yattle may be due to arrest of meiosis at about the pachytene stage [7]. Testes transcriptomics and proteomics show that downregulated genes primarily associated with meiosis and spermiogenesis are poorly expressed in sterile yattle [8,9].…”

Molecular characterization of the Yp11.2 region deletion in the Chinese Han population

“…TSPY is expressed only in testicular tissue and may be involved in spermatogenesis. Previous studies demonstrated that TSPY1 has physiological functions in the proliferation and differentiation of spermatogonia during spermatogenesis [ 15 ]. Remarkably, TSPY1 is also involved in the initiation and development of many tumors by activating the PI3K/AKT and RAS signaling pathways by suppressing IGFBP3 expression [ 16 ].…”

Cloning and Expression Analysis of Two Kdm Lysine Demethylases in the Testes of Mature Yaks and Their Sterile Hybrids

“…The H3K9me1 and H3K9me2 histone demethylase JMJD1A is essential for spermatogenesis [21]. Previous studies have suggested that it is important to consider the epigenetic perspective when conducting research on cattle-yak spermatogenesis aiming to explore the mechanisms of cattle-yak sterility [5,22,23].…”