Meiosis, a New Playground for Retrotransposon Evolution

Retrotransposons provide both threats and evolutionary opportunities for their hosts. In this issue of Developmental Cell, Laureau et al. describe a fascinating host-retrotransposon relationship that may lead to retrotransposon domestication: Ty3/Gypsy exploit meiosis networks sustain transcription, while the host deploys RNA-binding proteins prevent translation. genomes are engaged into forced union, in which respective interests have be constantly tempered allow long-term viable relationship. rely on cellular system multiplication, but they refrain from excessive exploitation propagation, as own success depends fitness. Conversely, organisms developed variety defense mechanisms, is likely key repurposing retrotransposons evolutionarily beneficial attributes. The conflict between most active germline. need expressed germ cells generate new heritable copies expand population wide. Reciprocally, continuously evolve counteracting mechanisms against protect integrity genetic material preserve fertility (Zamudio Bourc’his, 2010Zamudio N. Bourc’his D. Transposable elements mammalian germline: comfortable niche or deadly trap?.Heredity. 2010; 105: 92-104Crossref PubMed Scopus (111) Google Scholar). al., 2021Laureau R. Dyatel A. Dursuk G. Brown S. Adeoye H. Yue J.-X. De Chiara M. Harris Ünal E. Liti al.Meiotic counteract programmed activation via translational repressor assemblies.Dev. Cell. 2021; 56 (this issue): 22-35Abstract Full Text PDF (1) Scholar depict striking illustration an duel genomes: adopted sneaky strategy guarantee transcription during meiosis, meiotic use specialized stop resuming retrotransposition cycle. form group LTR (long terminal repeat) encode two proteins, Gag3 Gag3-Pol3, necessary structural enzymatic support Ty3 multiplication RNA intermediate. Laboratory strains Saccharomyces cerevisiae contain one full-length few dozen solo-LTRs. Without environmental challenges, low haploid cells. However, response pheromones, LTR-initiated highly stimulated mating cells, suggesting functional coupling expression reproduction. By applying sequencing (RNA-seq) northern blot analyses yeast synchronously progress through found also triggered at onset reach maximal mRNA levels metaphase first division. This temporality reminiscent targets master regulator Ndt80; indeed, single copy present strain authors study integrated downstream Ndt80 binding sites, its correlates with dose kinetics. sites act upstream activating sequences (UASs), initiated whose enhancing effect abolished upon increasing distance Ty3. Importantly, proximity was not oddity integrant specific strain; it recurrently observed distinct solo-LTR copies. conclude exploited regulatory specifically couple meiosis. novo integration events rare, suggests do leave unattended. Despite high levels, protein absent translation blocked by Rim4, assembles amyloid-like structures precocious required late only (Berchowitz 2013Berchowitz L.E. Gajadhar A.S. van Werven F.J. Rosa A.A. Samoylova M.L. Brar G.A. Xu Y. Xiao C. Futcher B. Weissman J.S. al.A developmentally regulated control pathway establishes chromosome segregation pattern.Genes Dev. 2013; 27: 2147-2163Crossref (49) Upon auxin-inducible Rim4 degradation, restored. Whether production Ty3-encoded sufficient complete assessed. It remains unclear whether full spectrum accessory mobilization cells—such nuclear pore components processing enzymes (Sandmeyer 2015Sandmeyer Patterson K. Bilanchone V. Ty3, position-specific budding yeast.Microbiol. Spectr. 2015; 3 (MDNA3-0057-2014)PubMed Scholar)—are diploid How targeted next obvious. what clear has direct advantage being integrants can transmitted mating. prevents happening within frame alleviated outside (Carpenter 2018Carpenter Bell R.B. Yunus J. Amon Berchowitz Phosphorylation-mediated clearance assemblies meiosis.Dev. 2018; 45: 392-405.e6Abstract (36) If some persists past sudden switch mitotic growth, could resumed occur. itself does seem immediately gain gametogenesis proceeds normally Ty3-deleted mutants. just tolerate it, because harmful. become challenging conditions lens evolution interesting question, went exploring. contrast yeast, no longer mobile genomes, many been domesticated genes fulfill useful functions (Naville 2016Naville Warren I.A. Haftek-Terreau Z. Chalopin Brunet F. Levin P. Galiana Volff J.-N. Not so bad after all: retroviruses long repeat source vertebrates.Clin. Microbiol. Infect. 2016; 22: 312-323Abstract (32) human genome, about hundred fragments Gypsy-related Gag (Campillos 2006Campillos Doerks T. Shah P.K. Bork Computational characterization multiple Gag-like proteins.Trends Genet. 2006; 585-589Abstract (89) Seminal examples include neuron-specific Arc gene involved synaptic plasticity (Pastuzyn 2018Pastuzyn E.D. Day C.E. Kearns Kyrke-Smith Taibi A.V. McCormick Yoder Belnap D.M. Erlendsson Morado D.R. al.The Neuronal Gene Encodes Repurposed Retrotransposon Protein Mediates Intercellular Transfer.Cell. 172: 275-288.e18Abstract (192) Scholar) Peg10 gene, product placentation (Youngson 2005Youngson N.A. Kocialkowski Peel Ferguson-Smith A.C. A small family sushi-class retrotransposon-derived mammals relation genomic imprinting.J. Mol. Evol. 2005; 61: 481-490Crossref (75) To check whether, similarly Gypsy relatives program analyzed RNA-seq data adult mouse testes. Two Gypsy-derived Gag-containing were identified actively transcribed spermatocytes, Moap1 Pnma1. Both belong Pnma (Paraneoplastic Ma antigens) family, expanded duplication reached 12 mice 15 humans analogy Ndt80, meiosis-specific factors STRA8 MYBL1—which entry progression, respectively—bind Pnma1 bound MYBL1. Accordingly, downregulated Stra8 Mybl1 mutant testes, mutants, supports these factors. mutants lack expressed, confounding effects exist. Further expanding model, checked if orthologs DAZ modulate mRNAs. Using available immunoprecipitation datasets, DAZL binds Gypsy-like sequence mRNAs testes associates MOAP1 PNMA1 fetal ovaries. They concluded co-option regulators conserved feature elements, well ability redirect toward male female germlines. Recruitment pre-dated allowed genes. Interestingly, brain, other Ty3/Gypsy-derived including Arc. More specifically, apoptosis neurons, overexpression contribute neurodegenerative disorders (Chen D’Mello, 2010Chen H.-L. D’Mello S.R. Induction neuronal cell death paraneoplastic Ma1 antigen.J. Neurosci. Res. 88: 3508-3519Crossref (22) participate regulation transcripts brain would path investigate, especially regarding propensity assemble aggregates outcomes. Meiotic Cells Counteract Programmed Activation RNA-Binding Translational Repressor AssembliesLaureau al.Developmental CellDecember 4, 2020In BriefRetrotransposon proliferation poses threat germline integrity. demonstrate LTR-retrotransposons co-opt factor gametogenesis. defense, developing gametes block Mammalian derived equivalent circuitry, host-transposon conflicts shape emerging function. Full-Text Open Access