The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis


In species that reproduce sexually, diploid individuals have two copies of each chromosome, inherited from their father and mother. During a special cell division called meiosis, these two sets of chromosomes are mixed by homologous recombination to give genetically unique chromosomes that will be transmitted to the next generation. Homologous recombination processes are highly controlled in terms of number and localization of events within and among chromosomes. Disruption of this control (a lack of or improper positioning of homologous recombination events) causes deleterious chromosome associations in the offspring. Using the model plant Arabidopsis thaliana we reveal here that the AtPSS1 gene is required for proper localization of these homologous recombination events along the genome. We also show that AtPSS1, which belongs to a family of proteins able to move along the cytoskeleton, is likely part of a module that allows cytoplasmic forces to be transmitted through the nucleus envelope to promote chromosome movements during homologous recombination progression.


Vyšlo v časopise: The Kinesin AtPSS1 Promotes Synapsis and is Required for Proper Crossover Distribution in Meiosis. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004674
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004674

Souhrn

In species that reproduce sexually, diploid individuals have two copies of each chromosome, inherited from their father and mother. During a special cell division called meiosis, these two sets of chromosomes are mixed by homologous recombination to give genetically unique chromosomes that will be transmitted to the next generation. Homologous recombination processes are highly controlled in terms of number and localization of events within and among chromosomes. Disruption of this control (a lack of or improper positioning of homologous recombination events) causes deleterious chromosome associations in the offspring. Using the model plant Arabidopsis thaliana we reveal here that the AtPSS1 gene is required for proper localization of these homologous recombination events along the genome. We also show that AtPSS1, which belongs to a family of proteins able to move along the cytoskeleton, is likely part of a module that allows cytoplasmic forces to be transmitted through the nucleus envelope to promote chromosome movements during homologous recombination progression.


Zdroje

1. MézardC, VignardJ, DrouaudJ, MercierR (2007) The road to crossovers: plants have their say. Trends Genet 23: 91–99 doi:10.1016/j.tig.2006.12.007

2. YoudsJL, BoultonSJ (2011) The choice in meiosis - defining the factors that influence crossover or non-crossover formation. J Cell Sci 124: 501–513 doi:10.1242/jcs.074427

3. NagaokaSI, HassoldTJ, HuntP (2012) Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet 13: 493–504 doi:10.1038/nrg3245

4. BerchowitzLE, CopenhaverGP (2010) Genetic interference: don't stand so close to me. Curr Genomics 11: 91–102 doi:10.2174/138920210790886835

5. MartiniE, DiazRL, HunterN, KeeneyS (2006) Crossover homeostasis in yeast meiosis. Cell 126: 285–295 doi:10.1016/j.cell.2006.05.044

6. YokooR, ZawadzkiKA, NabeshimaK, DrakeM, ArurS, et al. (2012) COSA-1 Reveals Robust Homeostasis and Separable Licensing and Reinforcement Steps Governing Meiotic Crossovers. Cell 149: 75–87 doi:10.1016/j.cell.2012.01.052

7. ColeF, KauppiL, LangeJ, RoigI, WangR, et al. (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14: 424–430 doi:10.1038/ncb2451

8. BaudatF, ImaiY, de MassyB (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14: 794–806 doi:10.1038/nrg3573

9. DrouaudJ, KhademianH, GirautL, ZanniV, BellalouS, et al. (2013) Contrasted Patterns of Crossover and Non-crossover at Arabidopsis thaliana Meiotic Recombination Hotspots. PLoS Genet 9: e1003922 doi:10.1371/journal.pgen.1003922

10. De MassyB (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet 47: 563–599 doi:10.1146/annurev-genet-110711-155423

11. GertonJL, HawleyRS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477–487 doi:10.1038/nrg1614

12. VignardJ, SiwiecT, ChelyshevaL, VrielynckN, GonordF, et al. (2007) The interplay of RecA-related proteins and the MND1-HOP2 complex during meiosis in Arabidopsis thaliana. PLoS Genet 3: 1894–1906 doi:10.1371/journal.pgen.0030176

13. CouteauF, BelzileF, HorlowC, GrandjeanO, VezonD, et al. (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11: 1623–1634.

14. De MuytA, PereiraL, VezonD, ChelyshevaL, GendrotG, et al. (2009) A high throughput genetic screen identifies new early meiotic recombination functions in Arabidopsis thaliana. PLoS Genet 5: e1000654 doi:10.1371/journal.pgen.1000654

15. WijnkerE, Velikkakam JamesG, DingJ, BeckerF, KlasenJR, et al. (2013) The genomic landscape of meiotic crossovers and gene conversions in Arabidopsis thaliana. Elife 2: e01426 doi:10.7554/eLife.01426

16. QiJ, WijeratneAJ, TomshoLP, HuY, SchusterSC, et al. (2009) Characterization of meiotic crossovers and gene conversion by whole-genome sequencing in Saccharomyces cerevisiae. BMC Genomics 10: 475 doi:10.1186/1471-2164-10-475

17. CifuentesM, RivardM, PereiraL, ChelyshevaL, MercierR (2013) Haploid meiosis in Arabidopsis: double-strand breaks are formed and repaired but without synapsis and crossovers. PLoS One 8: e72431 doi:10.1371/journal.pone.0072431

18. OsmanK, HigginsJD, Sanchez-MoranE, ArmstrongSJ, FranklinFCH (2011) Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol 190: 523–544 doi:10.1111/j.1469-8137.2011.03665.x

19. HarrisonCJ, AlveyE, HendersonIR (2010) Meiosis in flowering plants and other green organisms. J Exp Bot 61: 2863–2875 doi:10.1093/jxb/erq191

20. CromieGA, SmithGR (2007) Branching out: meiotic recombination and its regulation. Trends Cell Biol 17: 448–455 doi:10.1016/j.tcb.2007.07.007

21. LynnA, SoucekR, BörnerGV (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15: 591–605 doi:10.1007/s10577-007-1150-1

22. CrismaniW, GirardC, FrogerN, PradilloM, SantosJL, et al. (2012) FANCM limits meiotic crossovers. Science (80-) 336: 1588–1590 doi:10.1126/science.1220381

23. KnollA, HigginsJD, SeeligerK, RehaSJ, DangelNJ, et al. (2012) The Fanconi anemia ortholog FANCM ensures ordered homologous recombination in both somatic and meiotic cells in Arabidopsis. Plant Cell 24: 1448–1464 doi:10.1105/tpc.112.096644

24. KoszulR, KlecknerNE (2009) Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol 19: 716–724 doi:10.1016/j.tcb.2009.09.007

25. HiraokaY, DernburgAF (2009) The SUN rises on meiotic chromosome dynamics. Dev Cell 17: 598–605 doi:10.1016/j.devcel.2009.10.014

26. ChikashigeY, DingDQ, FunabikiH, HaraguchiT, MashikoS, et al. (1994) Telomere-led premeiotic chromosome movement in fission yeast. Science 264: 270–273.

27. ChikashigeY, TsutsumiC, YamaneM, OkamasaK, HaraguchiT, et al. (2006) Meiotic proteins bqt1 and bqt2 tether telomeres to form the bouquet arrangement of chromosomes. Cell 125: 59–69 doi:10.1016/j.cell.2006.01.048

28. SatoA, IsaacB, PhillipsCM, RilloR, CarltonPM, et al. (2009) Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139: 907–919 doi:10.1016/j.cell.2009.10.039

29. ShibuyaH, IshiguroK-I, WatanabeY (2014) The TRF1-binding protein TERB1 promotes chromosome movement and telomere rigidity in meiosis. Nat Cell Biol 16: 145–156 doi:10.1038/ncb2896

30. ScherthanH, WeichS, SchweglerH, HeytingC, HärleM, et al. (1996) Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J Cell Biol 134: 1109–1125.

31. SheehanMJ, PawlowskiWP (2009) Live imaging of rapid chromosome movements in meiotic prophase I in maize. Proc Natl Acad Sci U S A 106: 20989–20994 doi:10.1073/pnas.0906498106

32. ScherthanH (2001) A bouquet makes ends meet. Nat Rev Mol Cell Biol 2: 621–627 doi:10.1038/35085086

33. ChikashigeY, HaraguchiT, HiraokaY (2007) Another way to move chromosomes. Chromosoma 116: 497–505 doi:10.1007/s00412-007-0114-8

34. DingX, XuR, YuJ, XuT, ZhuangY, et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12: 863–872 doi:10.1016/j.devcel.2007.03.018

35. KoszulR, KimKP, PrentissM, KlecknerNE, KameokaS (2008) Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133: 1188–1201 doi:10.1016/j.cell.2008.04.050

36. ZicklerD, KlecknerNE (1998) The leptotene-zygotene transition of meiosis. Annu Rev Genet 32: 619–697 doi:10.1146/annurev.genet.32.1.619

37. RobertsNY, OsmanK, ArmstrongSJ (2009) Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana. Cytogenet Genome Res 124: 193–201 doi:10.1159/000218125

38. ZhouS, WangY, LiW, ZhaoZ, RenY, et al. (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23: 111–129 doi:10.1105/tpc.109.073692

39. RichardsonDN, SimmonsMP, ReddyASN (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7: 18 doi:10.1186/1471-2164-7-18

40. RossKJ, FranszP, JonesGH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosom Res 4: 507–516.

41. FerdousM, HigginsJD, OsmanK, LambingC, RoitingerE, et al. (2012) Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3. PLoS Genet 8: e1002507 doi:10.1371/journal.pgen.1002507

42. ArmstrongSJ, CarylAPP, JonesGH, FranklinFCH (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115: 3645–3655 doi:10.1242/jcs.00048

43. HigginsJD, Sanchez-MoranE, ArmstrongSJ, JonesGH, FranklinFCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19: 2488–2500 doi:10.1101/gad.354705

44. ChelyshevaL, VezonD, BelcramK, GendrotG, GrelonM (2008) The Arabidopsis BLAP75/Rmi1 homologue plays crucial roles in meiotic double-strand break repair. PLoS Genet 4: e1000309 doi:10.1371/journal.pgen.1000309

45. MotamayorJC, VezonD, BajonC, SauvanetA, GrandjeanO, et al. (2000) Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sex Plant Reprod 12: 209–218.

46. BerchowitzLE, CopenhaverGP (2008) Fluorescent Arabidopsis tetrads: a visual assay for quickly developing large crossover and crossover interference data sets. Nat Protoc 3: 41–50 doi:10.1038/nprot.2007.491

47. ChelyshevaL, GrandontL, VrielynckN, le GuinS, MercierR, et al. (2010) An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet Genome Res 129: 143–153 doi:10.1159/000314096

48. ChelyshevaL, VezonD, ChambonA, GendrotG, PereiraL, et al. (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet 8: e1002799 doi:10.1371/journal.pgen.1002799

49. HigginsJD, BucklingEF, FranklinFCH, JonesGH (2008) Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J 54: 152–162 doi:10.1111/j.1365-313X.2008.03403.x

50. BerchowitzLE, FrancisKE, BeyAL, CopenhaverGP (2007) The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet 3: e132 doi:10.1371/journal.pgen.0030132

51. EndowSa, KullFJ, LiuH (2010) Kinesins at a glance. J Cell Sci 123: 3420–3424 doi:10.1242/jcs.064113

52. ZhouX, GraumannK, EvansDE, MeierI (2012) Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J Cell Biol 196: 203–211 doi:10.1083/jcb.201108098

53. WicksteadB, GullK (2007) Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8: 1708–1721 doi:10.1111/j.1600-0854.2007.00646.x

54. TesséS, StorlazziA, KlecknerNE, GarganoS, ZicklerD (2003) Localization and roles of Ski8p protein in Sordaria meiosis and delineation of three mechanistically distinct steps of meiotic homolog juxtaposition. Proc Natl Acad Sci U S A 100: 12865–12870 doi:10.1073/pnas.2034282100

55. StorlazziA, GarganoS, Ruprich-RobertG, FalqueM, DavidM, et al. (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141: 94–106 doi:10.1016/j.cell.2010.02.041

56. ThackerD, MohibullahN, ZhuX, KeeneyS (2014) Homologue engagement controls meiotic DNA break number and distribution. Nature 510: 241–246 doi:10.1038/nature13120

57. KimKP, WeinerBM, ZhangL, JordanA, DekkerJ, et al. (2010) Sister cohesion and structural axis components mediate homolog bias of meiotic recombination. Cell 143: 924–937 doi:10.1016/j.cell.2010.11.015

58. LeeC-Y, ConradMN, DresserME (2012) Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 8: e1002730 doi:10.1371/journal.pgen.1002730

59. UanschouC, RonceretA, Von HarderM, De MuytA, VezonD, et al. (2013) Sufficient amounts of functional HOP2/MND1 complex promote interhomolog DNA repair but are dispensable for intersister DNA repair during meiosis in Arabidopsis. Plant Cell 25: 4924–4940 doi:10.1105/tpc.113.118521

60. KlecknerNE, ZicklerD, JonesGH, DekkerJ, PadmoreR, et al. (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci U S A 101: 12592–12597 doi:10.1073/pnas.0402724101

61. ZhangL, LiangZ, HutchinsonJ, KlecknerNE (2014) Crossover Patterning by the Beam-Film Model: Analysis and Implications. PLoS Genet 10: e1004042 doi:10.1371/journal.pgen.1004042

62. HigginsJD, VignardJ, MercierR, PughAG, FranklinFCH, et al. (2008) AtMSH5 partners AtMSH4 in the class I meiotic crossover pathway in Arabidopsis thaliana, but is not required for synapsis. Plant J 55: 28–39 doi:10.1111/j.1365-313X.2008.03470.x

63. ChelyshevaL, GendrotG, VezonD, DoutriauxM-P, MercierR, et al. (2007) Zip4/Spo22 is required for class I CO formation but not for synapsis completion in Arabidopsis thaliana. PLoS Genet 3: e83 doi:10.1371/journal.pgen.0030083

64. Francis, LamSY, HarrisonBD, BeyAL, BerchowitzLE, et al. (2007) Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci U S A 104: 3913–3918 doi:10.1073/pnas.0608936104

65. CromerL, JolivetS, HorlowC, ChelyshevaL, HeymanJ, et al. (2013) Centromeric cohesion is protected twice at meiosis, by SHUGOSHINs at anaphase I and by PATRONUS at interkinesis. Curr Biol 23: 2090–2099 doi:10.1016/j.cub.2013.08.036

66. VoinnetO, RivasS, MestreP, BaulcombeD (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949–956.

67. PerkinsDD (1949) Biochemical Mutants in the Smut Fungus Ustilago Maydis. Genetics 34: 607–626.

68. AlexanderMP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44: 117–122.

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