Conserved Meiotic Mechanisms in the Cnidarian Revealed by Knockout

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2023 Jan 27

PMID 36706182

Authors

Catriona Munro

Hugo Cadis

Sophie Pagnotta

Evelyn Houliston

Jean-Rene Huynh

Affiliations

Soon will be listed here.

Abstract

During meiosis, DNA recombination allows the shuffling of genetic information between the maternal and paternal chromosomes. Recombination is initiated by double-strand breaks (DSBs) catalyzed by the conserved enzyme Spo11. How this crucial event is connected to other meiotic processes is unexpectedly variable depending on the species. Here, we knocked down by CRISPR in the jellyfish . Germ cells in mutants fail to assemble synaptonemal complexes and chiasmata, and in consequence, homologous chromosome pairs in females remain unassociated during oocyte growth and meiotic divisions, creating aneuploid but fertilizable eggs that develop into viable larvae. thus shares an ancient eukaryotic dependence of synapsis and chromosome segregation on Spo11-generated DSBs. Phylogenetically, belongs to Cnidaria, the sister clade to Bilateria where classical animal model species are found, so these results provide fresh evolutionary perspectives on meiosis regulation.

Citing Articles

VitelloTag: a tool for high-throughput cargo delivery into oocytes.

Clarke D, Kane A, Perillo M, Lowe C, Swartz S Development. 2024; 151(20).

PMID: 39171380 PMC: 11423919. DOI: 10.1242/dev.202857.

The genome of the colonial hydroid reveals that their stem cells use a toolkit of evolutionarily shared genes with all animals.

Schnitzler C, Chang E, Waletich J, Quiroga-Artigas G, Wong W, Nguyen A Genome Res. 2024; 34(3):498-513.

PMID: 38508693 PMC: 11067881. DOI: 10.1101/gr.278382.123.

Epithelial wound healing in Clytia hemisphaerica provides insights into extracellular ATP signaling mechanisms and P2XR evolution.

Lee E, OMalley-Krohn I, Edsinger E, Wu S, Malamy J Sci Rep. 2023; 13(1):18819.

PMID: 37914720 PMC: 10620158. DOI: 10.1038/s41598-023-45424-5.

Genetic and Epigenetic Regulation of Oocyte Determination.

Cabrita B, Martinho R J Dev Biol. 2023; 11(2).

PMID: 37367475 PMC: 10299578. DOI: 10.3390/jdb11020021.

References

Klapholz S, Waddell C, Esposito R . The role of the SPO11 gene in meiotic recombination in yeast. Genetics. 1985; 110(2):187-216. PMC: 1202559. DOI: 10.1093/genetics/110.2.187. View

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

Celerin M, Merino S, Stone J, Menzie A, Zolan M . Multiple roles of Spo11 in meiotic chromosome behavior. EMBO J. 2000; 19(11):2739-50. PMC: 212740. DOI: 10.1093/emboj/19.11.2739. View

Zickler D, Kleckner N . Recombination, Pairing, and Synapsis of Homologs during Meiosis. Cold Spring Harb Perspect Biol. 2015; 7(6). PMC: 4448610. DOI: 10.1101/cshperspect.a016626. View

Storlazzi A, Tesse S, Gargano S, James F, Kleckner N, Zickler D . Meiotic double-strand breaks at the interface of chromosome movement, chromosome remodeling, and reductional division. Genes Dev. 2003; 17(21):2675-87. PMC: 280617. DOI: 10.1101/gad.275203. View

Keeney S, Giroux C, Kleckner N . Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997; 88(3):375-84. DOI: 10.1016/s0092-8674(00)81876-0. View

Fraune J, Alsheimer M, Volff J, Busch K, Fraune S, Bosch T . Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans. Proc Natl Acad Sci U S A. 2012; 109(41):16588-93. PMC: 3478637. DOI: 10.1073/pnas.1206875109. View

Christophorou N, Rubin T, Bonnet I, Piolot T, Arnaud M, Huynh J . Microtubule-driven nuclear rotations promote meiotic chromosome dynamics. Nat Cell Biol. 2015; 17(11):1388-400. DOI: 10.1038/ncb3249. View

McKim K . mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev. 1998; 12(18):2932-42. PMC: 317166. DOI: 10.1101/gad.12.18.2932. View

10.

Romanienko P, Camerini-Otero R . The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell. 2000; 6(5):975-87. DOI: 10.1016/s1097-2765(00)00097-6. View

11.

Petronczki M, Siomos M, Nasmyth K . Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell. 2003; 112(4):423-40. DOI: 10.1016/s0092-8674(03)00083-7. View

12.

Jessus C, Munro C, Houliston E . Managing the Oocyte Meiotic Arrest-Lessons from Frogs and Jellyfish. Cells. 2020; 9(5). PMC: 7290932. DOI: 10.3390/cells9051150. View

13.

Blokhina Y, Nguyen A, Draper B, Burgess S . The telomere bouquet is a hub where meiotic double-strand breaks, synapsis, and stable homolog juxtaposition are coordinated in the zebrafish, Danio rerio. PLoS Genet. 2019; 15(1):e1007730. PMC: 6336226. DOI: 10.1371/journal.pgen.1007730. View

14.

Rubin T, Macaisne N, Valles A, Guilleman C, Gaugue I, Dal Toe L . Premeiotic pairing of homologous chromosomes during male meiosis. Proc Natl Acad Sci U S A. 2022; 119(47):e2207660119. PMC: 9704699. DOI: 10.1073/pnas.2207660119. View

15.

Goodenough U, Heitman J . Origins of eukaryotic sexual reproduction. Cold Spring Harb Perspect Biol. 2014; 6(3). PMC: 3949356. DOI: 10.1101/cshperspect.a016154. View

16.

MacQueen A, Phillips C, Bhalla N, Weiser P, Villeneuve A, Dernburg A . Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell. 2005; 123(6):1037-50. PMC: 4435800. DOI: 10.1016/j.cell.2005.09.034. View

17.

Sinigaglia C, Thiel D, Hejnol A, Houliston E, Leclere L . A safer, urea-based in situ hybridization method improves detection of gene expression in diverse animal species. Dev Biol. 2017; 434(1):15-23. DOI: 10.1016/j.ydbio.2017.11.015. View

18.

Rillo-Bohn R, Adilardi R, Mitros T, Avsaroglu B, Stevens L, Kohler S . Analysis of meiosis in reveals plasticity in homolog pairing and synapsis in the nematode lineage. Elife. 2021; 10. PMC: 8455136. DOI: 10.7554/eLife.70990. View

19.

Guo L, Accorsi A, He S, Guerrero-Hernandez C, Sivagnanam S, McKinney S . An adaptable chromosome preparation methodology for use in invertebrate research organisms. BMC Biol. 2018; 16(1):25. PMC: 5828064. DOI: 10.1186/s12915-018-0497-4. View

20.

Baudat F, Manova K, Yuen J, Jasin M, Keeney S . Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol Cell. 2000; 6(5):989-98. DOI: 10.1016/s1097-2765(00)00098-8. View