Teleosts are unique among vertebrates, with a wide range of haploid genome sizes in very close lineages, varying from less than 400 mega base pairs (Mb) for pufferfish to over 3000 Mb for salmon. The cause of the difference in genome size remains largely unexplained. In this study, we reveal that the differential success of transposable elements (TEs) correlates with the variation of genome size across four representative teleost species (zebrafish, medaka, stickleback, and tetraodon). The larger genomes represent a higher diversity within each clade (superfamily) and family and a greater abundance of TEs compared with the smaller genomes; zebrafish, representing the largest genome, shows the highest diversity and abundance of TEs in its genome, followed by medaka and stickleback; while the tetraodon, representing the most compact genome, displays the lowest diversity and density of TEs in its genome. Both of Class I (retrotransposons) and Class II TEs (DNA transposons) contribute to the difference of TE accumulation of teleost genomes, however, Class II TEs are the major component of the larger teleost genomes analyzed and the most important contributors to genome size variation across teleost lineages. The hAT and Tc1/Mariner superfamilies are the major DNA transposons of all four investigated teleosts. Divergence distribution revealed contrasting proliferation dynamics both between clades of retrotransposons and between species. The TEs within the larger genomes of the zebrafish and medaka represent relatively stronger activity with an extended time period during the evolution history, in contrast with the very young activity in the smaller stickleback genome, or the very low level of activity in the tetraodon genome. Overall, our data shows that teleosts represent contrasting profiles of mobilomes with a differential density, diversity and activity of TEs. The differences in TE accumulation, dominated by DNA transposons, explain the main size variations of genomes across the investigated teleost species, and the species differences in both diversity and activity of TEs contributed to the variations of TE accumulations across the four teleost species. TEs play major roles in teleost genome evolution.

Mumps virus (MuV) has high tropism to the testis and may lead to male infertility. Sertoli cells are the major targets of MuV infection. However, the mechanisms by which MuV infection impairs male fertility and Sertoli cell function remain unclear. The present study elucidated the effect of MuV infection on the blood‐testis barrier (BTB). The transepithelial electrical resistance of MuV‐infected mouse Sertoli cells was monitored, and the expression of major proteins of the BTB was examined. We demonstrated that MuV infection disrupted the BTB by reducing the levels of occludin and zonula occludens 1. Sertoli cells derived from Tlr2 ^–/– and Tnfa ^–/– mice were analyzed for mediating MuV‐induced impairment. TLR2‐mediated TNF‐α production by Sertoli cells in response to MuV infection impaired BTB integrity. MuV‐impaired BTB was not observed in Tlr2 ^–/– and Tnfa ^–/– Sertoli cells. Moreover, an inhibitor of TNF‐α, pomalidomide, prevents the disruption of BTB in response to MuV infection. FITC‐labeled biotin tracing assay confirmed that BTB permeability and spermatogenesis were transiently impaired by MuV infection in vivo . These findings suggest that the disruption of the BTB could be one of the mechanisms underlying MuV‐impaired male fertility, in which TNF‐α could play a critical role.—Wu, H., Jiang, X., Gao, Y., Liu, W., Wang, F., Gong, M., Chen, R., Yu, X., Zhang, W., Gao, B., Song, C., Han, D. Mumps virus infection disrupts blood‐testis barrier through the induction of TNF‐α in Sertoli cells. FASEB J. 33, 12528–12540 (2019). www.fasebj.org

S: Background: Tc1/mariner and Zator, as two superfamilies of IS630-Tc1-mariner (ITm) group, have been well-defined. However, the molecular evolution and domestication of pogo transposons, once designated as an important family of the Tc1/mariner superfamily, are still poorly understood. Results: Here, phylogenetic analysis show that pogo transposases, together with Tc1/mariner, DD34E/Gambol, and Zator transposases form four distinct monophyletic clades with high bootstrap supports (> = 74%), suggesting that they are separate superfamilies of ITm group. The pogo superfamily represents high diversity with six distinct families (Passer, Tigger, pogoR, Lemi, Mover, and Fot/Fot-like) and wide distribution with an expansion spanning across all the kingdoms of eukaryotes. It shows widespread occurrences in animals and fungi, but restricted taxonomic distribution in land plants. It has invaded almost all lineages of animals—even mammals—and has been domesticated repeatedly in vertebrates, with 12 genes, including centromere-associated protein B (CENPB), CENPB DNA-binding domain containing 1 (CENPBD1), Jrk helix–turn–helix protein (JRK), JRK like (JRKL), pogo transposable element derived with KRAB domain (POGK), and with ZNF domain (POGZ), and Tigger transposable element-derived 2 to 7 (TIGD2–7), deduced as originating from this superfamily. Two of them (JRKL and TIGD2) seem to have been co-domesticated, and the others represent independent domestication events. Four genes (TIGD3, TIGD4, TIGD5, and POGZ) tend to represent ancient domestications in vertebrates, while the others only emerge in mammals and seem to be domesticated recently. Significant structural variations including target site duplication (TSD) types and the DDE triad signatures (DD29–56D) were observed for pogo transposons. Most domesticated genes are derived from the complete transposase genes; but CENPB, POGK, and POGZ are chimeric genes fused with additional functional domains. Conclusions: This is the first report to systematically reveal the evolutionary profiles of the pogo transposons, suggesting that pogo and Tc1/Mariner are two separate superfamilies of ITm group, and demonstrating the repeated domestications of pogo in vertebrates. These data indicate that pogo transposons have played important roles in shaping the genome and gene evolution of fungi and animals. This study expands our understanding of the diversity of pogo transposons and updates the classification of ITm group.

The similarities and differences of small RNAs in seminal plasma, epididymal sperm and ejaculated sperm remain largely undefined. We conducted a systematic comparative analysis of small RNA profiles in pig ejaculated sperm, epididymal sperm and seminal plasma and found that the diversity distribution of small RNA species was generally similar, whereas the abundance of small RNAs is dramatically different across the three libraries; miRNAs and small RNAs derived from rRNA, tRNA, small nuclear RNA, 7SK RNA, NRON RNA and cis-regulatory RNA were enriched in the three libraries, but piRNA was absent. A large population of small RNAs from ejaculated sperm are ejaculated sperm specific, and only 8–30% of small RNAs overlapped with those of epididymal sperm or seminal plasma and a small proportion (5–18%) of small RNAs were shared in the three libraries, suggesting that, in addition to the testes, sperm RNAs may also originate from seminal plasma, epididymis as well as other resources. Most miRNAs were co-distributed but differentially expressed across the three libraries, with epididymal sperm exhibiting the highest abundance, followed by ejaculated sperm and seminal plasma. The prediction of target genes of the top 10 highly expressed miRNAs across the three libraries revealed that these miRNAs may be involved in spermatogenesis, zygote development and the interaction between the environment and animals. Our study provides the first description of the similarities and differences of small RNA profiles in ejaculated sperm, epididymal sperm and seminal plasma and indicates that sperm RNA may have origins other than the testes.

Retrotransposons are the major determinants of genome sizes and they have shaped both genes and genomes in mammalian organisms, but their overall activity, diversity, and evolution dynamics, particularly their impact on protein coding and lncRNA genes in pigs remain largely unknown. In the present study, we performed de novo detection of retrotransposons in pigs by using multiple pipelines, four distinct families of pig-specific L1 s classified into 51 distinct subfamilies and representing four evolution models and three expansion waves of pig-specific SINEs represented by three distinct families were identified. ERVs were classified into 18 families and found two most “modern” subfamilies in the pig genome. The transposition activity of pig L1 was verified by experiment, the sense and antisense promoter activities of young L1 5′UTRs and ERV LTRs and expression profiles of young retrotransposons in multiple tissues and cell lines were also validated. Furthermore, retrotransposons had an extensive impact on lncRNA and protein coding genes at both the genomic and transcriptomic levels. Most protein coding and lncRNA (> 80%) genes contained retrotransposon insertions, and about half of protein coding genes (44.30%) and one-fourth (24.13%) of lncRNA genes contained the youngest retrotransposon insertions. Nearly half of protein coding genes (43.78%) could generate chimeric transcripts with retrotransposons. Significant distribution bias of retrotransposon composition, location, and orientation in lncRNA and protein coding genes, and their transcripts, were observed. In the current study, we characterized the classification and evolution profile of retrotransposons in pigs, experimentally proved the transposition activity of the young pig L1 subfamily, characterized the sense and antisense expression profiles and promoter activities of young retrotransposons, and investigated their impact on lncRNA and protein coding genes by defining the mobilome landscapes at the genomic and transcriptomic levels. These findings help provide a better understanding of retrotransposon evolution in mammal and their impact on the genome and transcriptome.