1932

Abstract

Comparisons among a variety of eukaryotes have revealed considerable variability in the structures and processes involved in their meiosis. Nevertheless, conventional forms of meiosis occur in all major groups of eukaryotes, including early-branching protists. This finding confirms that meiosis originated in the common ancestor of all eukaryotes and suggests that primordial meiosis may have had many characteristics in common with conventional extant meiosis. However, it is possible that the synaptonemal complex and the delicate crossover control related to its presence were later acquisitions. Later still, modifications to meiotic processes occurred within different groups of eukaryotes. Better knowledge on the spectrum of derived and uncommon forms of meiosis will improve our understanding of many still mysterious aspects of the meiotic process and help to explain the evolutionary basis of functional adaptations to the meiotic program.

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2016-11-23
2024-06-20
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Literature Cited

  1. Albini SM, Jones GH. 1.  1987. Synaptonemal complex spreading in Allium cepa and A. fistulosum. I. The initiation and sequence of pairing. Chromosoma 95:324–38 [Google Scholar]
  2. Aldrich HC, Mims CW. 2.  1970. Synaptonemal complexes and meiosis in Myxomycetes. Am. J. Bot. 57:935–41 [Google Scholar]
  3. Archetti M. 3.  2004. Loss of complementation and the logic of two-step meiosis. J. Evol. Biol. 17:1098–1105 [Google Scholar]
  4. Barthel D, Detmer A. 4.  1990. The spermatogenesis of Halichondria panicea (Porifera, Demospongiae). Zoomorphology 110:9–15 [Google Scholar]
  5. Beam CA, Himes M. 5.  1980. Sexuality and meiosis in dinoflagellates. Biochemistry and Physiology of Protozoa 3 M Levandowsky, SH Hutner 171–206 New York: Academic, 2nd ed.. [Google Scholar]
  6. Belar K. 6.  1922. Untersuchungen an Actinophrys sol Ehrenberg. I. Die Morphologie des Formwechsels. Arch. Protistenkd. 46:1–96 [Google Scholar]
  7. Bloomfield G. 7.  2016. Atypical ploidy cycles, Spo11, and the evolution of meiosis. Semin. Cell Dev. Biol. 54:158–64 [Google Scholar]
  8. Bomblies K, Higgins JD, Yant L. 8.  2015. Meiosis evolves: adaptation to external and internal environments. New Phytol 208:306–23 [Google Scholar]
  9. Börner GV, Kleckner N, Hunter N. 9.  2004. Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45 [Google Scholar]
  10. Braselton JP. 10.  1982. Karyotype analysis of Plasmodiophora brassicae based on serial thin sections of pachytene nuclei. Can. J. Bot. 60:403–8 [Google Scholar]
  11. Bråten T, Nordby Ø. 11.  1973. Ultrastructure of meiosis and centriole behaviour in Ulva mutabilis Føyn. J. Cell Sci. 13:69–81 [Google Scholar]
  12. Brown MS, Bishop DK. 12.  2015. DNA strand exchange and RecA homologs in meiosis. Cold Spring Harb. Perspect. Biol. 7:a016659 [Google Scholar]
  13. Bull JJ, Harvey PH. 13.  1989. A new reason for having sex. Nature 339:260–61 [Google Scholar]
  14. Burki F. 14.  2014. The eukaryotic tree of life from a global phylogenomic perspective. Cold Spring Harb. Perspect. Biol. 6:a016147 [Google Scholar]
  15. Cabral G, Marques A, Schubert V, Pedrosa-Harand A, Schlögelhofer P. 15.  2014. Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes. Nat. Commun. 5:5070 [Google Scholar]
  16. Carpenter ML, Assaf ZJ, Gourguechon S, Cande WZ. 16.  2012. Nuclear inheritance and genetic exchange without meiosis in the binucleate parasite Giardia intestinalis. J. Cell Sci. 125:2523–32 [Google Scholar]
  17. Carr M, Leadbeater BSC, Baldauf SL. 17.  2010. Conserved meiotic genes point to sex in the choanoflagellates. J. Eukaryot. Microbiol. 57:56–62 [Google Scholar]
  18. Cavalier-Smith T. 18.  1995. Cell cycles, diplokaryosis and the archezoan origin of sex. Arch. Protistenkd. 145:189–207 [Google Scholar]
  19. Chapman JR, Taylor MRG, Boulton SJ. 19.  2012. Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47:497–510 [Google Scholar]
  20. Charlot F, Chelysheva L, Kamisugi Y, Vrielynck N, Guyon A. 20.  et al. 2014. RAD51B plays an essential role during somatic and meiotic recombination in Physcomitrella. Nucleic Acids Res. 42:11965–78 [Google Scholar]
  21. Chi J, Mahé F, Loidl J, Logsdon J, Dunthorn M. 21.  2014. Meiosis gene inventory of four ciliates reveals the prevalence of a synaptonemal complex-independent crossover pathway. Mol. Biol. Evol. 31:660–72 [Google Scholar]
  22. Chi J, Parrow MW, Dunthorn M. 22.  2014. Cryptic sex in Symbiodinium (Alveolata, Dinoflagellata) is supported by an inventory of meiotic genes. J. Eukaryot. Microbiol. 61:322–27 [Google Scholar]
  23. Christophorou N, Rubin T, Bonnet I, Piolot T, Arnaud M, Huynh J-R. 23.  2015. Microtubule-driven nuclear rotations promote meiotic chromosome dynamics. Nat. Cell Biol. 17:1388–1400 [Google Scholar]
  24. Cleveland LR. 24.  1947. The origin and evolution of meiosis. Science 105:287–89 [Google Scholar]
  25. Clutterbuck AJ. 25.  1996. Parasexual recombination in fungi. J. Genet. 75:281–86 [Google Scholar]
  26. Crown KN, Savytskyy OP, Malik SB, Logsdon J, Williams RS. 26.  et al. 2013. A mutation in the FHA domain of Coprinus cinereus Nbs1 leads to Spo11-independent meiotic recombination and chromosome segregation. G3 3:1927–43 [Google Scholar]
  27. Da Ines O, White CI. 27.  2015. Centromere associations in meiotic chromosome pairing. Annu. Rev. Genet. 49:95–114 [Google Scholar]
  28. Darlington CD. 28.  1937. Recent Advances in Cytology Philadelphia: Blakiston's, 2nd ed.. [Google Scholar]
  29. de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM. 29.  2003. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164:81–94 [Google Scholar]
  30. de Massy B. 30.  2013. Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu. Rev. Genet. 47:563–99 [Google Scholar]
  31. del Cacho E, Pages M, Gallego M, Monteagudo L, Sánchez-Acedo C. 31.  2005. Synaptonemal complex karyotype of Eimeria tenella. Int. J. Parasitol. 35:1445–51 [Google Scholar]
  32. Dernburg AF, Sedat JW, Hawley RS. 32.  1996. Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86:135–46 [Google Scholar]
  33. Devidé Z, Geitler L. 33.  1947. Die Chromosomen der Ciliaten. Chromosoma 3:110–36 [Google Scholar]
  34. Egel R, Penny D. 34.  2008. On the origin of meiosis in eukaryotic evolution: coevolution of meiosis and mitosis from feeble beginnings. Recombination and Meiosis R Egel, D-H Lankenau 249–88 Genome Dyn. Stab. Ser. 3 Berlin: Springer-Verlag [Google Scholar]
  35. Egel-Mitani M, Olson LW, Egel R. 35.  1982. Meiosis in Aspergillus nidulans: another example for lacking synaptonemal complexes in the absence of crossover interference. Hereditas 97:179–87 [Google Scholar]
  36. Farah JA, Cromie G, Davis L, Steiner WW, Smith GR. 36.  2005. Activation of an alternative, rec12 (Spo11)-independent pathway of fission yeast meiotic recombination in the absence of a DNA flap endonuclease. Genetics 171:1499–511 [Google Scholar]
  37. Figueroa RI, Cuadrado A, Stüken A, Rodríguez F, Fraga S. 37.  2014. Ribosomal DNA organization patterns within the dinoflagellate genus Alexandrium as revealed by FISH: life cycle and evolutionary implications. Protist 165:343–63 [Google Scholar]
  38. Figueroa RI, Rengefors K, Bravo I. 38.  2006. Effects of parental factors and meiosis on sexual offspring of Gymnodinium nolleri (Dinophyceae). J. Phycol. 42:350–62 [Google Scholar]
  39. Flegel TW, Pasharawipas T. 39.  1995. A proposal for typical eukaryotic meiosis in microsporidians. Can. J. Microbiol. 41:1–11 [Google Scholar]
  40. Forche A, Alby K, Schaefer D, Johnson AD, Berman J, Bennett RJ. 40.  2008. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLOS Biol 6:e110 [Google Scholar]
  41. Fowler KR, Gutiérrez-Velasco S, Martín-Castellanos C, Smith GR. 41.  2013. Protein determinants of meiotic DNA break hot spots. Mol. Cell 49:983–96 [Google Scholar]
  42. Fraune J, Wiesner M, Benavente R. 42.  2014. The synaptonemal complex of basal metazoan Hydra: more similarities to vertebrate than invertebrate meiosis model organisms. J. Genet. Genom. 41:107–15 [Google Scholar]
  43. Gladyshev E, Kleckner N. 43.  2014. Direct recognition of homology between double helices of DNA in Neurospora crassa. Nat. Commun. 5:3509 [Google Scholar]
  44. Glöckner G, Hülsmann N, Schleicher M, Noegel AA, Eichinger L. 44.  et al. 2014. The genome of the foraminiferan Reticulomyxa filosa. Curr. Biol. 24:1–8 [Google Scholar]
  45. Godward MBE. 45.  1966. The Chromosomes of the Algae London: Edward Arnold Ltd. [Google Scholar]
  46. Golczyk H, Massouh A, Greiner S. 46.  2014. Translocations of chromosome end-segments and facultative heterochromatin promote meiotic ring formation in evening primroses. Plant Cell 26:1280–93 [Google Scholar]
  47. Goldfarb T, Lichten M. 47.  2010. Frequent and efficient use of the sister chromatid for DNA double-strand break repair during budding yeast meiosis. PLOS Biol 8:e1000520 [Google Scholar]
  48. Grishaeva TM, Bogdanov YF. 48.  2014. Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes. Int. J. Evol. Biol. 2014:856230 [Google Scholar]
  49. Haig D. 49.  1993. Alternatives to meiosis: the unusual genetics of red algae, microsoporidia, and others. J. Theor. Biol. 163:15–31 [Google Scholar]
  50. Hanke-Bücker G, Hauser M. 50.  1996. Nuclear phenomena during conjugation of the suctorian Heliophrya erhardi: I. EM-observations of micronuclear meiosis. Eur. J. Protistol. 32:459–80 [Google Scholar]
  51. Harris SE, Braselton JP, Miller CE. 51.  1980. Chromosomal number of Sorosphaera veronicae (Plasmodiophoromycetes) based on ultrastructural analysis of synaptonemal complexes. Mycologia 72:916–25 [Google Scholar]
  52. Hazard EI, Brookbank JW. 52.  1984. Karyogamy and meiosis in an Ambylospora sp. (Microspora) in the mosquito Culex salinarius. J. Invert. Pathol 44:3–11 [Google Scholar]
  53. He D, Fiz-Palacios O, Fu C-J, Fehling J, Tsai C-C, Baldauf SL. 53.  2014. An alternative root for the eukaryote tree of life. Curr. Biol. 24:465–70 [Google Scholar]
  54. Heckmann S, Jankowska M, Schubert V, Kumke K, Ma W, Houben A. 54.  2014. Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans. Nat. Commun. 5:4979 [Google Scholar]
  55. Heywood P, Magee PT. 55.  1976. Meiosis in protists. Some structural and physiological aspects of meiosis in algae, fungi, and protozoa. Bacteriol. Rev. 40:190–240 [Google Scholar]
  56. Himes M, Beam CA. 56.  1975. Genetic analysis in the dinoflagellate Crypthecodinium (Gyrodinium) cohnii: evidence for unusual meiosis. PNAS 72:4546–49 [Google Scholar]
  57. Hiraoka Y, Dernburg AF. 57.  2009. The SUN rises on meiotic chromosome dynamics. Dev. Cell 17:598–605 [Google Scholar]
  58. Hollande A, Carruette-Valentin J. 58.  1970. Appariement chromosomique et complexes synaptonématiques dans les noyaux en cours de déploidisation chez Pyrsonympha flagellata: le cycle évolutif des Pyrsonymphines symbiontes de Reticulitermes lucifugus. C. R. Acad. Sci. D 270:2550–53 [Google Scholar]
  59. Howard-Till RA, Lukaszewicz A, Novatchkova M, Loidl J. 59.  2013. A single cohesin complex performs mitotic and meiotic functions in the protist Tetrahymena. PLOS Genet 9:e1003418 [Google Scholar]
  60. Hughes SE, Hawley RS. 60.  2014. Topoisomerase II is required for the proper separation of heterochromatic regions during Drosophila melanogaster female meiosis. PLOS Genet 10:e1004650 [Google Scholar]
  61. Hurst LD, Nurse P. 61.  1991. A note on the evolution of meiosis. J. Theor. Biol. 150:561–63 [Google Scholar]
  62. Ito BM, Takegami MH, Noda S. 62.  1983. Achiasmate meiosis in the Fritillaria japonica group II. Formation of synaptinemal complexes in microsporocytes. Jpn. J. Genet. 58:377–81 [Google Scholar]
  63. John B. 63.  1990. Meiosis Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  64. Joyce EF, Williams BR, Xie T, Wu CT. 64.  2012. Identification of genes that promote or antagonize somatic homolog pairing using a high-throughput FISH-based screen. PLOS Genet 8:e1002667 [Google Scholar]
  65. Kelso AA, Say AF, Sharma D, Ledford LL, Turchick A. 65.  et al. 2015. Entamoeba histolytica Dmc1 catalyzes homologous DNA pairing and strand exchange that is stimulated by calcium and Hop2-Mnd1. PLOS ONE 10:e0139399 [Google Scholar]
  66. Kohl KP, Sekelsky J. 66.  2013. Meiotic and mitotic recombination in meiosis. Genetics 194:327–34 [Google Scholar]
  67. Kondrashov AS. 67.  1997. Evolutionary genetics of life cycles. Annu. Rev. Ecol. Syst. 28:391–435 [Google Scholar]
  68. Krishnan B, Thomas SE, Yan RH, Yamada H, Zhulin IB, McKee BD. 68.  2014. Sisters unbound is required for meiotic centromeric cohesion in Drosophila melanogaster. Genetics 198:947–65 [Google Scholar]
  69. Kugrens P, West JA. 69.  1972. Synaptonemal complexes in red algae. J. Phycol. 8:187–91 [Google Scholar]
  70. Lam I, Keeney S. 70.  2014. Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb. Perspect. Biol. 7:a016634 [Google Scholar]
  71. Lécher P. 71.  1978. The synaptonemal complex in the bipartition division of the radiolaria Aulacantha scolymantha. Can. J. Genet. Cytol. 20:85–95 [Google Scholar]
  72. Lee C-Y, Conrad MN, Dresser ME. 72.  2012. Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLOS Genet 8:e1002730 [Google Scholar]
  73. Lee C-Y, Horn HF, Stewart CL, Burke B, Bolcun-Filas E. 73.  et al. 2015. Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes. Cell Rep 11:551–63 [Google Scholar]
  74. Lee JY, Terakawa T, Qi Z, Steinfeld JB, Redding S. 74.  et al. 2015. Base triplet stepping by the Rad51/RecA family of recombinases. Science 349:977–81 [Google Scholar]
  75. Li XX, Dawe RK. 75.  2009. Fused sister kinetochores initiate the reductional division in meiosis I. Nat. Cell Biol. 11:1103–8 [Google Scholar]
  76. Lie T, Laane MM. 76.  1982. Reconstruction analyses of synaptonemal complexes in haploid and diploid pachytene nuclei of Physarum polycephalum (Myxomycetes). Hereditas 96:119–40 [Google Scholar]
  77. Loidl J. 77.  1990. The initiation of meiotic chromosome pairing: the cytological view. Genome 33:759–78 [Google Scholar]
  78. Loidl J. 78.  2006. S. pombe linear elements: the modest cousins of synaptonemal complexes. Chromosoma 115:260–71 [Google Scholar]
  79. Loidl J, Lorenz A. 79.  2016. DNA double-strand break formation and repair in Tetrahymena meiosis. Sem. Cell Dev. Biol. 54:126–34 [Google Scholar]
  80. Loidl J, Lukaszewicz A, Howard-Till RA, Koestler T. 80.  2012. The Tetrahymena meiotic chromosome bouquet is organized by centromeres and promotes interhomolog recombination. J. Cell Sci. 125:5873–80 [Google Scholar]
  81. Loidl J, Mochizuki K. 81.  2009. Tetrahymena meiotic nuclear reorganization is induced by a checkpoint kinase-dependent response to DNA damage. Mol. Biol. Cell 20:2428–37 [Google Scholar]
  82. Lorenz A, Fuchs J, Bürger R, Loidl J. 82.  2003. Chromosome pairing does not contribute to nuclear architecture in vegetative yeast cells. Eukaryot. Cell 2:856–66 [Google Scholar]
  83. Lorenz A, Wells JL, Pryce DW, Novatchkova M, Eisenhaber F. 83.  et al. 2004. S. pombe meiotic linear elements contain proteins related to synaptonemal complex components. J. Cell Sci. 117:3343–51 [Google Scholar]
  84. Lynn A, Soucek R, Börner V. 84.  2007. ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15:591–605 [Google Scholar]
  85. Lynn DH. 85.  2008. The Ciliated Protozoa. Characterization, Classification and Guide to the Literature Dordrecht, Neth.: Springer [Google Scholar]
  86. Macinnes MA, Francis D. 86.  1974. Meiosis in Dictyostelium mucoroides. Nature 251:321–24 [Google Scholar]
  87. Maguire MP. 87.  1992. The evolution of meiosis. J. Theor. Biol. 154:43–55 [Google Scholar]
  88. Mann DG, Stickle AJ. 88.  1989. Meiosis, nuclear cyclosis, and auxospore formation in Navicula sensu stricto (Bacillariophyta). Brit. Phycol. J. 24:167–81 [Google Scholar]
  89. Manton I, Kowallik K, von Stosch HA. 89.  1969. Observations on the fine structure and development of the spindle at mitosis and meiosis in a marine centric diatom (Lithodesmium undulatum). II. The early meiotic stages in male gametogenesis. J. Cell Sci. 5:271–98 [Google Scholar]
  90. Mark Welch JL, Mark Welch DB, Meselson M. 90.  2004. Cytogenetic evidence for asexual evolution of bdelloid rotifers. PNAS 101:1618–21 [Google Scholar]
  91. Melters DP, Paliulis LV, Korf IF, Chan SWL. 91.  2012. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res 20:579–93 [Google Scholar]
  92. Mézard C, Jahns MT, Grelon M. 92.  2015. Where to cross? New insights into the location of meiotic crossovers. Trends Genet 31:393–401 [Google Scholar]
  93. Mignot J-P. 93.  1980. Étude ultrastructurale de la pédogamie chez Actinophrys sol (Héliozoaire). II. Les divisions de maturation. Protistologica 16:205–25 [Google Scholar]
  94. Miyoshi T, Ito M, Ohta T. 94.  2013. Spatiotemporal regulation of meiotic recombination by Liaisonin. Bioarchitecture 3:20–24 [Google Scholar]
  95. Mlambo G, Coppens I, Kumar N. 95.  2012. Aberrant sporogonic development of Dmc1 (a meiotic recombinase) deficient Plasmodium berghei parasites. PLOS ONE 7:e52480 [Google Scholar]
  96. Moens PB, Perkins FO. 96.  1969. Chromosome number of a small protist: accurate determination. Science 166:1289–91 [Google Scholar]
  97. Nasmyth K. 97.  2015. A meiotic mystery: how sister kinetochores avoid being pulled in opposite directions during the first division. BioEssays 37:657–65 [Google Scholar]
  98. Nassonova ES, Smirnov AV. 98.  2005. Synaptonemal complexes as evidence for meiosis in the life cycle of the monomorphic diplokaryotic microsporidium Paranosema grylli. Eur. J. Protistol. 41:175–81 [Google Scholar]
  99. Nokkala S, Kuznetsova VG, Maryanska-Nadachowska A, Nokkala C. 99.  2006. Holocentric chromosomes in meiosis. II. The modes of orientation and segregation of a trivalent. Chromosome Res 14:559–65 [Google Scholar]
  100. Normark BB, Judson OP, Moran NA. 100.  2003. Genomic signatures of ancient asexual lineages. Biol. J. Linn. Soc. 79:69–84 [Google Scholar]
  101. Oakley HA, Jones GH. 101.  1982. Meiosis in Mesostoma ehrenbergii ehrenbergii (Turbellaria, Rhabdocoela). I. Chromosome pairing, synaptonemal complexes and chiasma localisation in spermatogenesis. Chromosoma 85:311–22 [Google Scholar]
  102. Obeso D, Pezza RJ, Dawson D. 102.  2014. Couples, pairs, and clusters: mechanisms and implications of centromere associations in meiosis. Chromosoma 123:43–55 [Google Scholar]
  103. Patil S, Moeys S, von Dassow P, Huysman MJJ, Mapleson D. 103.  et al. 2015. Identification of the meiotic toolkit in diatoms and exploration of meiosis-specific SPO11 and RAD51 homologs in the sexual species Pseudo-nitzschia multistriata and Seminavis robusta. BMC Genom 16:930 [Google Scholar]
  104. Peacock L, Bailey M, Carrington M, Gibson W. 104.  2014. Meiosis and haploid gametes in the pathogen Trypanosoma brucei. Curr. Biol. 24:181–86 [Google Scholar]
  105. Petronczki M, Siomos MF, Nasmyth K. 105.  2003. Un ménage à quatre: the molecular biology of chromosome segregation in meiosis. Cell 112:423–40 [Google Scholar]
  106. Pfiester LA, Timpano P, Skvarla JJ, Holt JR. 106.  1984. Sexual reproduction and meiosis in Peridinium inconspicuum Lemmermann (Dinophyceae). Amer. J. Bot. 71:1121–27 [Google Scholar]
  107. Phadnis N, Hyppa RW, Smith GR. 107.  2011. New and old ways to control meiotic recombination. Trends Genet 27:411–21 [Google Scholar]
  108. Phillips CM, Dernburg AF. 108.  2006. A family of zinc-finger proteins is required for chromosome-specific pairing and synapsis during meiosis in C. elegans. Dev. Cell 11:817–29 [Google Scholar]
  109. Poxleitner MK, Carpenter ML, Mancuso JJ, Wang C-JR, Dawson SC, Cande WZ. 109.  2008. Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science 319:1530–33 [Google Scholar]
  110. Raikov IB. 110.  1982. The Protozoan Nucleus: Morphology and Evolution Vienna: Springer-Verlag [Google Scholar]
  111. Raikov IB. 111.  1995. Meiosis in protists: recent advances and persisting problems. Eur. J. Protistol. 31:1–7 [Google Scholar]
  112. Ramesh MA, Malik S-B, Logsdon JM Jr. 112.  2005. A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15:185–91 [Google Scholar]
  113. Rasmussen SW. 113.  1973. Ultrastructural studies of spermatogenesis in Drosophila melanogaster Meigen. Z. Zellforsch. 140:125–44 [Google Scholar]
  114. Ray C Jr. 114.  1956. Meiosis and nuclear behaviour in Tetrahymena pyriformis. J. Protozool. 3:88–96 [Google Scholar]
  115. Rog O, Dernburg AF. 115.  2013. Chromosome pairing and synapsis during Caenorhabditis elegans meiosis. Curr. Opin. Cell Biol. 25:349–56 [Google Scholar]
  116. San Filippo J, Sung P, Klein H. 116.  2008. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77:229–57 [Google Scholar]
  117. Scherthan H. 117.  2001. A bouquet makes ends meet. Nat. Rev. Mol. Cell Biol. 2:621–27 [Google Scholar]
  118. Schurko AM, Logsdon JM Jr. 118.  2008. Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. BioEssays 30:579–89 [Google Scholar]
  119. Serrentino ME, Borde V. 119.  2012. The spatial regulation of meiotic recombination hotspots: Are all DSB hotspots crossover hotspots?. Exp. Cell Res. 318:1347–52 [Google Scholar]
  120. Severson AF, Meyer BJ. 120.  2014. Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes. eLife 3:e03467 [Google Scholar]
  121. Shibuya H, Watanabe Y. 121.  2014. The meiosis specific modification of mammalian telomeres. Cell Cycle 13:2024–28 [Google Scholar]
  122. Shodhan A, Lukaszewicz A, Novatchkova M, Loidl J. 122.  2014. Msh4 and Msh5 function in SC-independent chiasma formation during the streamlined meiosis of Tetrahymena. Genetics 198:983–93 [Google Scholar]
  123. Singh N, Bhattacharya A, Bhattacharya S. 123.  2013. Homologous recombination occurs in Entamoeba and is enhanced during growth stress and stage conversion. PLOS ONE 8:e74465 [Google Scholar]
  124. Sinden RE, Hartley RH. 124.  1985. Identification of the meiotic division of malarial parasites. J. Protozool. 32:742–44 [Google Scholar]
  125. Soyer-Gobillard MO, Bhaud Y, Saint Hilaire D. 125.  2002. New data on mating in an autotrophic dinoflagellate, Prorocentrum micans Ehrenberg. Vie Milieu 52:167–75 [Google Scholar]
  126. Speijer D, Lukeš J, Eliáš M. 126.  2015. Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. PNAS 112:8827–34 [Google Scholar]
  127. Stack SM, Soulliere DL. 127.  1984. The relation between synapsis and chiasma formation in Rhoeo spathacea. Chromosoma 90:72–83 [Google Scholar]
  128. Storms R, Hastings PJ. 128.  1977. A fine structure analysis of meiotic pairing in Chlamydomonas reinhardi. Exp. Cell Res. 104:39–46 [Google Scholar]
  129. Subramanian VV, Hochwagen A. 129.  2011. Centromere clustering: where synapsis begins. Curr. Biol. 21:R920–22 [Google Scholar]
  130. Tachibana-Konwalski K. 130.  2015. Cell division: hold on and let go. Nature 517:441–42 [Google Scholar]
  131. Takeo S, Lake CM, Morais-de-Sá E, Sunkel CE, Hawley RS. 131.  2011. Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr. Biol. 21:1845–51 [Google Scholar]
  132. Tanneti SN, Landy K, Joyce EF, McKim KS. 132.  2011. A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr. Biol. 21:1852–57 [Google Scholar]
  133. Thomas SE, Soltani-Bejnood M, Roth P, Dorn R, Logsdon JM Jr., McKee BD. 133.  2005. Identification of two proteins required for conjunction and regular segregation of achiasmate homologs in Drosophila male meiosis. Cell 123:555–68 [Google Scholar]
  134. Tillmann U, Hoppenrath M. 134.  2013. Life cycle of the pseudocolonial dinoflagellate Polykrikos kofoidii (Gymnodiales, Dinoflagellata). J. Phycol. 49:298–317 [Google Scholar]
  135. Toth R, Markey DR. 135.  1973. Synaptonemal complexes in brown algae. Nature 243:236–37 [Google Scholar]
  136. Tsai J-H, McKee BD. 136.  2011. Homologous pairing and the role of pairing centers in meiosis. J. Cell Sci. 124:1955–63 [Google Scholar]
  137. Tsubouchi T, MacQueen AJ, Roeder GS. 137.  2008. Initiation of meiotic chromosome synapsis at centromeres in budding yeast. Genes Dev 22:3217–26 [Google Scholar]
  138. Varas J, Graumann K, Osman K, Pradillo M, Evans DE. 138.  et al. 2015. Absence of SUN1 and SUN2 proteins in Arabidopsis thaliana leads to a delay in meiotic progression and defects in synapsis and recombination. Plant J 81:329–46 [Google Scholar]
  139. Viera A, Page J, Rufas JS. 139.  2009. Inverted meiosis: the true bugs as a model to study. Meiosis R Benavente, J-N Volff 137–56 Genome Dyn. Ser. 5 Basel, Switz.: Karger [Google Scholar]
  140. Villeneuve AM, Hillers KJ. 140.  2001. Whence meiosis?. Cell 106:647–50 [Google Scholar]
  141. von Stosch HA. 141.  1973. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates, Gymondinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. Br. Phycol. J 8:105–34 [Google Scholar]
  142. von Wettstein D, Rasmussen SW, Holm PB. 142.  1984. The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18:331–413 [Google Scholar]
  143. Whitby MC. 143.  2005. Making crossovers during meiosis. Biochem. Soc. Trans. 33:1451–55 [Google Scholar]
  144. Wilkins AS, Holliday R. 144.  2009. The evolution of meiosis from mitosis. Genetics 181:3–12 [Google Scholar]
  145. Wolfe J, Hunter B, Adair WS. 145.  1976. A cytological study of micronuclear elongation during conjugation in Tetrahymena. Chromosoma 55:289–308 [Google Scholar]
  146. Xiang YB, Miller DE, Ross EJ, Sánchez-Alvarado A, Hawley RS. 146.  2014. Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea. PNAS 111:E5159–68 [Google Scholar]
  147. Youds JL, Boulton SJ. 147.  2011. The choice in meiosis—defining the factors that influence crossover or non-crossover formation. J. Cell Sci. 124:501–13 [Google Scholar]
  148. Zakharyevich K, Tang S, Ma Y, Hunter N. 148.  2012. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149:334–47 [Google Scholar]
  149. Zhang J, Pawlowski WP, Han FP. 149.  2013. Centromere pairing in early meiotic prophase requires active centromeres and precedes installation of the synaptonemal complex in maize. Plant Cell 25:3900–9 [Google Scholar]
  150. Zhao DZ, Yang XH, Quan L, Timofejeva L, Rigel NW. 150.  et al. 2006. ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis. Plant Mol. Biol. 62:99–110 [Google Scholar]
  151. Zickler D. 151.  2006. From early homologue recognition to synaptonemal complex formation. Chromosoma 115:158–74 [Google Scholar]
  152. Zickler D, Kleckner N. 152.  1999. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. 33:603–754 [Google Scholar]
  153. Zickler D, Kleckner N. 153.  2015. Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb. Perspect. Biol. 7:a016626 [Google Scholar]
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