Evolutionary Innovations in Germline Biology of Placental Mammals Identified by Transcriptomics of First-wave Spermatogenesis in Opossum

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2024 Nov 13

PMID 39536760

Authors

Kira L Marshall

Daniel J Stadtmauer

Jamie Maziarz

Gunter P Wagner

Bluma J Lesch

Affiliations

Soon will be listed here.

Abstract

Mammalian spermatogenesis is a highly stereotyped and conserved developmental process that is essential for fitness. At the same time, gene expression in spermatogenic cells is rapidly evolving. This combination of features has been suggested to drive rapid fixation of new gene expression patterns. Using a high-resolution dataset comprising bulk and single-cell data from juvenile and adult testes of the opossum Monodelphis domestica, a model marsupial, we define the developmental timing of the spermatogenic first wave in opossum and delineate conserved and divergent gene expression programs across the placental-marsupial split by comparison to equivalent data from mouse, a model placental mammal. Epigenomic data confirmed divergent regulation at the level of transcription, and comparison to data from four additional amniote species identified hundreds of genes with evidence of rapid fixation of expression. This gene set encompasses known and previously undescribed regulators of spermatogenic development.

References

Kawamura K, Kumagai J, Sudo S, Chun S, Pisarska M, Morita H . Paracrine regulation of mammalian oocyte maturation and male germ cell survival. Proc Natl Acad Sci U S A. 2004; 101(19):7323-8. PMC: 409917. DOI: 10.1073/pnas.0307061101. View

Prabhakar S, Visel A, Akiyama J, Shoukry M, Lewis K, Holt A . Human-specific gain of function in a developmental enhancer. Science. 2008; 321(5894):1346-50. PMC: 2658639. DOI: 10.1126/science.1159974. View

Najle S, Grau-Bove X, Elek A, Navarrete C, Cianferoni D, Chiva C . Stepwise emergence of the neuronal gene expression program in early animal evolution. Cell. 2023; 186(21):4676-4693.e29. PMC: 10580291. DOI: 10.1016/j.cell.2023.08.027. View

Pertea M, Kim D, Pertea G, Leek J, Salzberg S . Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc. 2016; 11(9):1650-67. PMC: 5032908. DOI: 10.1038/nprot.2016.095. View

Badia-I-Mompel P, Velez Santiago J, Braunger J, Geiss C, Dimitrov D, Muller-Dott S . decoupleR: ensemble of computational methods to infer biological activities from omics data. Bioinform Adv. 2023; 2(1):vbac016. PMC: 9710656. DOI: 10.1093/bioadv/vbac016. View

Durinck S, Spellman P, Birney E, Huber W . Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat Protoc. 2009; 4(8):1184-91. PMC: 3159387. DOI: 10.1038/nprot.2009.97. View

Fayomi A, Orwig K . Spermatogonial stem cells and spermatogenesis in mice, monkeys and men. Stem Cell Res. 2018; 29:207-214. PMC: 6010318. DOI: 10.1016/j.scr.2018.04.009. View

Xu K, Su X, Fang K, Lv Y, Huang T, Li M . The Slingshot phosphatase 2 is required for acrosome biogenesis during spermatogenesis in mice. Elife. 2023; 12. PMC: 10065795. DOI: 10.7554/eLife.83129. View

Lynch V, Tanzer A, Wang Y, Leung F, Gellersen B, Emera D . Adaptive changes in the transcription factor HoxA-11 are essential for the evolution of pregnancy in mammals. Proc Natl Acad Sci U S A. 2008; 105(39):14928-33. PMC: 2567470. DOI: 10.1073/pnas.0802355105. View

10.

Uebbing S, Kunstner A, Makinen H, Backstrom N, Bolivar P, Burri R . Divergence in gene expression within and between two closely related flycatcher species. Mol Ecol. 2016; 25(9):2015-28. PMC: 4879514. DOI: 10.1111/mec.13596. View

11.

Butler C, Shaw G, Clark J, Renfree M . The functional development of Leydig cells in a marsupial. J Anat. 2007; 212(1):55-66. PMC: 2423388. DOI: 10.1111/j.1469-7580.2007.00837.x. View

12.

Kent W, Zweig A, Barber G, Hinrichs A, Karolchik D . BigWig and BigBed: enabling browsing of large distributed datasets. Bioinformatics. 2010; 26(17):2204-7. PMC: 2922891. DOI: 10.1093/bioinformatics/btq351. View

13.

Zhang M, Wang X, Yao J, Qiu Z . Long non-coding RNA NEAT1 inhibits oxidative stress-induced vascular endothelial cell injury by activating the miR-181d-5p/CDKN3 axis. Artif Cells Nanomed Biotechnol. 2019; 47(1):3129-3137. DOI: 10.1080/21691401.2019.1646264. View

14.

Ramirez F, Ryan D, Gruning B, Bhardwaj V, Kilpert F, Richter A . deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 2016; 44(W1):W160-5. PMC: 4987876. DOI: 10.1093/nar/gkw257. View

15.

Esteban-Lopez M, Agoulnik A . Diverse functions of insulin-like 3 peptide. J Endocrinol. 2020; 247(1):R1-R12. PMC: 7453995. DOI: 10.1530/JOE-20-0168. View

16.

Bao J, Rousseaux S, Shen J, Lin K, Lu Y, Bedford M . The arginine methyltransferase CARM1 represses p300•ACT•CREMτ activity and is required for spermiogenesis. Nucleic Acids Res. 2018; 46(9):4327-4343. PMC: 5961101. DOI: 10.1093/nar/gky240. View

17.

FRANK L . Effects of oxygen on the newborn. Fed Proc. 1985; 44(7):2328-34. View

18.

Lau X, Munusamy P, Ng M, Sangrithi M . Single-Cell RNA Sequencing of the Cynomolgus Macaque Testis Reveals Conserved Transcriptional Profiles during Mammalian Spermatogenesis. Dev Cell. 2020; 54(4):548-566.e7. DOI: 10.1016/j.devcel.2020.07.018. View

19.

Swanson W, Vacquier V . The rapid evolution of reproductive proteins. Nat Rev Genet. 2002; 3(2):137-44. DOI: 10.1038/nrg733. View

20.

Chirn G, Rahman R, Sytnikova Y, Matts J, Zeng M, Gerlach D . Conserved piRNA Expression from a Distinct Set of piRNA Cluster Loci in Eutherian Mammals. PLoS Genet. 2015; 11(11):e1005652. PMC: 4654475. DOI: 10.1371/journal.pgen.1005652. View