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Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis


Autoři: Spencer G. Gordon aff001;  Lisa E. Kursel aff001;  Kewei Xu aff001;  Ofer Rog aff001
Působiště autorů: School of Biological Sciences, University of Utah, Salt Lake City, Utah, United States of America aff001
Vyšlo v časopise: Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis. PLoS Genet 17(3): e1009205. doi:10.1371/journal.pgen.1009205
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009205

Souhrn

During sexual reproduction the parental homologous chromosomes find each other (pair) and align along their lengths by integrating local sequence homology with large-scale contiguity, thereby allowing for precise exchange of genetic information. The Synaptonemal Complex (SC) is a conserved zipper-like structure that assembles between the homologous chromosomes, bringing them together and regulating exchanges between them. However, the molecular mechanisms by which the SC carries out these functions remain poorly understood. Here we isolated and characterized two mutations in the dimerization interface in the middle of the SC zipper in C. elegans. The mutations perturb both chromosome alignment and the regulation of genetic exchanges. Underlying the chromosome-scale phenotypes are distinct alterations to the way SC subunits interact with one another. We propose a model whereby the SC brings homologous chromosomes together through two activities: obligate zipping that prevents assembly on unpaired chromosomes; and a tendency to extend pairing interactions along the entire length of the chromosomes.

Klíčová slova:

Caenorhabditis elegans – Crossover interference – Gonads – Homologous chromosomes – Chromosome pairs – Sequence alignment – Synapsis – X chromosomes


Zdroje

1. Rog O. and Dernburg A.F., Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr Opin Cell Biol, 2013. 25(3): p. 349–56. PMC3694717 doi: 10.1016/j.ceb.2013.03.003 23578368

2. Rog O. and Dernburg A.F., Direct Visualization Reveals Kinetics of Meiotic Chromosome Synapsis. Cell Rep, 2015. PMC4565782 doi: 10.1016/j.celrep.2015.02.032 25772351

3. Page S.L. and Hawley R.S., The genetics and molecular biology of the synaptonemal complex. Annu Rev Cell Dev Biol, 2004. 20: p. 525–58. doi: 10.1146/annurev.cellbio.19.111301.155141 15473851

4. Libuda D.E., et al., Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature, 2013. 502(7473): p. 703–6. PMC3920622 doi: 10.1038/nature12577 24107990

5. Woglar A. and Villeneuve A.M., Dynamic Architecture of DNA Repair Complexes and the Synaptonemal Complex at Sites of Meiotic Recombination. Cell, 2018. 173(7): p. 1678–1691 e16. PMC6003859 doi: 10.1016/j.cell.2018.03.066 29754818

6. Cahoon C.K., Helm J.M., and Libuda D.E., Synaptonemal Complex Central Region Proteins Promote Localization of Pro-crossover Factors to Recombination Events During Caenorhabditis elegans Meiosis. Genetics, 2019. 213(2): p. 395–409. PMC6781886 doi: 10.1534/genetics.119.302625 31431470

7. MacQueen A.J., et al., Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev, 2002. 16(18): p. 2428–42. PMC187442 doi: 10.1101/gad.1011602 12231631

8. Colaiacovo M.P., et al., Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. Dev Cell, 2003. 5(3): p. 463–74. doi: 10.1016/s1534-5807(03)00232-6 12967565

9. Smolikov S., Schild-Prufert K., and Colaiacovo M.P., A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet, 2009. 5(10): p. e1000669. PMC2742731 doi: 10.1371/journal.pgen.1000669 19798442

10. Smolikov S., et al., SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics, 2007. 176(4): p. 2015–25. PMC1950610 doi: 10.1534/genetics.107.072413 17565948

11. Hurlock M.E., et al., Identification of novel synaptonemal complex components in C. elegans. J Cell Biol, 2020. 219(5). PMC7199856 doi: 10.1083/jcb.201910043 32211899

12. Zhang Z., et al., Multivalent weak interactions between assembly units drive synaptonemal complex formation. J Cell Biol, 2020. 219(5). PMC7199860 doi: 10.1083/jcb.201910086 32211900

13. Köhler S., et al., The interaction of crossover formation and the dynamic architecture of the synaptonemal complex during meiosis. bioRxiv, 2020: p. 2020.02.16.947804.

14. Schucker K., et al., Elucidation of synaptonemal complex organization by super-resolution imaging with isotropic resolution. Proc Natl Acad Sci U S A, 2015. 112(7): p. 2029–33. PMC4343094 doi: 10.1073/pnas.1414814112 25646409

15. Schild-Prufert K., et al., Organization of the synaptonemal complex during meiosis in Caenorhabditis elegans. Genetics, 2011. 189(2): p. 411–21. PMC3189812 doi: 10.1534/genetics.111.132431 21840865

16. Dunce J.M., et al., Structural basis of meiotic chromosome synapsis through SYCP1 self-assembly. Nat Struct Mol Biol, 2018. 25(7): p. 557–569. PMC6606445 doi: 10.1038/s41594-018-0078-9 29915389

17. Rog O., Kohler S., and Dernburg A.F., The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors. Elife, 2017. 6. PMC5268736 doi: 10.7554/eLife.21455 28045371

18. Pattabiraman D., et al., Meiotic recombination modulates the structure and dynamics of the synaptonemal complex during C. elegans meiosis. PLoS Genet, 2017. 13(3): p. e1006670. PMC5384771 doi: 10.1371/journal.pgen.1006670 28339470

19. Sym M. and Roeder G.S., Zip1-induced changes in synaptonemal complex structure and polycomplex assembly. J Cell Biol, 1995. 128(4): p. 455–66. PMC2199901 doi: 10.1083/jcb.128.4.455 7860625

20. Ollinger R., Alsheimer M., and Benavente R., Mammalian protein SCP1 forms synaptonemal complex-like structures in the absence of meiotic chromosomes. Mol Biol Cell, 2005. 16(1): p. 212–7. PMC539165 doi: 10.1091/mbc.e04-09-0771 15496453

21. Billmyre K.K., et al., X chromosome and autosomal recombination are differentially sensitive to disruptions in SC maintenance. Proc Natl Acad Sci U S A, 2019. 116(43): p. 21641–21650. PMC6815145 doi: 10.1073/pnas.1910840116 31570610

22. Jeffress J.K., et al., The formation of the central element of the synaptonemal complex may occur by multiple mechanisms: the roles of the N- and C-terminal domains of the Drosophila C(3)G protein in mediating synapsis and recombination. Genetics, 2007. 177(4): p. 2445–56. PMC2219479 doi: 10.1534/genetics.107.078717 17947423

23. Tung K.S. and Roeder G.S., Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics, 1998. 149(2): p. 817–32. PMC1460213 9611194

24. Voelkel-Meiman K., et al., Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSgamma-Mediated Crossover Formation. Genetics, 2016. 203(3): p. 1091–103. PMC4937465 doi: 10.1534/genetics.115.182923 27184389

25. Voelkel-Meiman K., et al., Crossover recombination and synapsis are linked by adjacent regions within the N terminus of the Zip1 synaptonemal complex protein. PLoS Genet, 2019. 15(6): p. e1008201. PMC6605668 doi: 10.1371/journal.pgen.1008201 31220082

26. Roelens B., et al., Spatial Regulation of Polo-Like Kinase Activity During Caenorhabditis elegans Meiosis by the Nucleoplasmic HAL-2/HAL-3 Complex. Genetics, 2019. 213(1): p. 79–96. PMC6727811 doi: 10.1534/genetics.119.302479 31345995

27. Zhang W., et al., HAL-2 promotes homologous pairing during Caenorhabditis elegans meiosis by antagonizing inhibitory effects of synaptonemal complex precursors. PLoS Genet, 2012. 8(8): p. e1002880. PMC3415444 doi: 10.1371/journal.pgen.1002880 22912597

28. Sato-Carlton A., et al., Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation. J Cell Biol, 2018. 217(2): p. 555–570. PMC5800814 doi: 10.1083/jcb.201707161 29222184

29. Garcia-Muse T., et al., A Meiotic Checkpoint Alters Repair Partner Bias to Permit Inter-sister Repair of Persistent DSBs. Cell Rep, 2019. 26(3): p. 775–787 e5. PMC6334227 doi: 10.1016/j.celrep.2018.12.074 30650366

30. Gao J., et al., N-terminal acetylation promotes synaptonemal complex assembly in C. elegans. Genes Dev, 2016. 30(21): p. 2404–2416. PMC5131780 doi: 10.1101/gad.277350.116 27881602

31. Phillips C.M., et al., HIM-8 binds to the X chromosome pairing center and mediates chromosome-specific meiotic synapsis. Cell, 2005. 123(6): p. 1051–63. PMC4435792 doi: 10.1016/j.cell.2005.09.035 16360035

32. Hayashi M., Mlynarczyk-Evans S., and Villeneuve A.M., The synaptonemal complex shapes the crossover landscape through cooperative assembly, crossover promotion and crossover inhibition during Caenorhabditis elegans meiosis. Genetics, 2010. 186(1): p. 45–58. PMC2940310 doi: 10.1534/genetics.110.115501 20592266

33. Harper N.C., et al., Pairing centers recruit a Polo-like kinase to orchestrate meiotic chromosome dynamics in C. elegans. Dev Cell, 2011. 21(5): p. 934–47. PMC4343031 doi: 10.1016/j.devcel.2011.09.001 22018922

34. Phillips C.M. and Dernburg A.F., A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev Cell, 2006. 11(6): p. 817–29. doi: 10.1016/j.devcel.2006.09.020 17141157

35. MacQueen A.J., et al., Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell, 2005. 123(6): p. 1037–50. PMC4435800 doi: 10.1016/j.cell.2005.09.034 16360034

36. Hughes S.E., et al., The E3 ubiquitin ligase Sina regulates the assembly and disassembly of the synaptonemal complex in Drosophila females. PLoS Genet, 2019. 15(5): p. e1008161. PMC6544331 doi: 10.1371/journal.pgen.1008161 31107865

37. Goodyer W., et al., HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell, 2008. 14(2): p. 263–74. doi: 10.1016/j.devcel.2007.11.016 18267094

38. Couteau F., et al., A component of C. elegans meiotic chromosome axes at the interface of homolog alignment, synapsis, nuclear reorganization, and recombination. Curr Biol, 2004. 14(7): p. 585–92. doi: 10.1016/j.cub.2004.03.033 15062099

39. Wang K., et al., Increasing the Genetic Recombination Frequency by Partial Loss of Function of the Synaptonemal Complex in Rice. Mol Plant, 2015. 8(8): p. 1295–8. doi: 10.1016/j.molp.2015.04.011 25936677

40. Yokoo R., et al., COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell, 2012. 149(1): p. 75–87. PMC3339199 doi: 10.1016/j.cell.2012.01.052 22464324

41. Almanzar D.E., Gordon S.G., and Rog O., Meiotic sister chromatid exchanges are rare in C. elegans. bioRxiv, 2020: p. 2020.07.22.216614.

42. Tsai C.J., et al., Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev, 2008. 22(2): p. 194–211. PMC2192754 doi: 10.1101/gad.1618508 18198337

43. Rockman M.V. and Kruglyak L., Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet, 2009. 5(3): p. e1000419. PMC2652117 doi: 10.1371/journal.pgen.1000419 19283065

44. Carlton P.M., Farruggio A.P., and Dernburg A.F., A link between meiotic prophase progression and crossover control. PLoS Genet, 2006. 2(2): p. e12. PMC1359072 APF performed the experiments. PMC, APF, and AFD analyzed the data. PMC and AFD wrote the paper. doi: 10.1371/journal.pgen.0020012 16462941

45. Li Q., et al., The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans. PLoS Genet, 2018. 14(11): p. e1007701. PMC6211623 doi: 10.1371/journal.pgen.1007701 30383767

46. Alberti S., Gladfelter A., and Mittag T., Considerations and Challenges in Studying Liquid-Liquid Phase Separation and Biomolecular Condensates. Cell, 2019. 176(3): p. 419–434. PMC6445271 doi: 10.1016/j.cell.2018.12.035 30682370

47. Pak C.W., et al., Sequence Determinants of Intracellular Phase Separation by Complex Coacervation of a Disordered Protein. Mol Cell, 2016. 63(1): p. 72–85. PMC4973464 doi: 10.1016/j.molcel.2016.05.042 27392146

48. Brenner S., The genetics of Caenorhabditis elegans. Genetics, 1974. 77(1): p. 71–94. PMC1213120 4366476

49. El Mouridi S., et al., Reliable CRISPR/Cas9 Genome Engineering in Caenorhabditis elegans Using a Single Efficient sgRNA and an Easily Recognizable Phenotype. G3 (Bethesda), 2017. 7(5): p. 1429–1437. PMC5427500 doi: 10.1534/g3.117.040824 28280211

50. Phillips C.M., McDonald K.L., and Dernburg A.F., Cytological analysis of meiosis in Caenorhabditis elegans. Methods Mol Biol, 2009. 558: p. 171–95. PMC3644504 doi: 10.1007/978-1-60761-103-5_11 19685325

51. Altschul S.F., et al., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res, 1997. 25(17): p. 3389–402. PMC146917 doi: 10.1093/nar/25.17.3389 9254694

52. Larkin M.A., et al., Clustal W and Clustal X version 2.0. Bioinformatics, 2007. 23(21): p. 2947–8. doi: 10.1093/bioinformatics/btm404 17846036

53. Clamp M., et al., The Jalview Java alignment editor. Bioinformatics, 2004. 20(3): p. 426–7. doi: 10.1093/bioinformatics/btg430 14960472

54. McDonnell A.V., et al., Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics, 2006. 22(3): p. 356–8. doi: 10.1093/bioinformatics/bti797 16317077

55. Kreher J., et al., Distinct Roles of Two Histone Methyltransferases in Transmitting H3K36me3-Based Epigenetic Memory Across Generations in Caenorhabditis elegans. Genetics, 2018. 210(3): p. 969–982. PMC6218224. doi: 10.1534/genetics.118.301353 30217796


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