Meiosis: Inducing Variation by Reduction

Abstract

A brief introduction is presented with some thought on the origin of meiosis. Subsequently, a sequential overview of the diverse processes that take place during meiosis is provided, with an eye to similarities and differences between the different eukaryotic systems. In the final part, we try to summarize the available core meiotic mutants and make a comprehensive comparison for orthologous genes between fungal, plant, and animal systems.

Pairing - synapsis - meiotic recombination - segregation - meiotic mutants.

References

• 1 Agashe B., Prasad C. K., Siddiqi I.. Identification and analysis of DYAD: a gene required for meiotic chromosome organization and female meiotic progression in Arabidopsis. .  Development. (2002);  129 3935-3943
• 2 Albini S. M., Jones G. H.. Synaptonemal complex spreading in Allium cepa and A. fistulosum. I. The initiation and sequence of pairing.  Chromosoma. (1987);  95 324-338
• 3 Allers T., Lichten M.. Differential timing and control of noncrossover and crossover recombination during meiosis.  Cell. (2001);  106 47-57
• 4 Amon A.. The spindle checkpoint.  Current Opinion in Genetics and Development. (1999);  9 69-75
• 5 Armstrong S. J., Christopher F., Franklin H., Jones G. H.. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. .  Journal of Cell Science. (2001);  114 4207-4217
• 6 Aragon-Alcaide L., Reader S., Beven A., Shaw P., Miller T., Moore G.. Association of homologous chromosomes during floral development.  Current Biology. (1997);  7 905-908
• 7 Armstrong S. J., Jones G. H.. Female meiosis in wild-type Arabidopsis thaliana and in two meiotic mutants.  Sexual Plant Reproduction. (2001);  13 177-183
• 8 Armstrong S. J., Franklin F. C. H., Jones G. H.. A meiotic time-course for Arabidopsis thaliana. .  Sexual Plant Reproduction. (2003);  16 141-149
• 9 Armstrong S. J., Jones G. H.. Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. .  Journal of Experimental Botany. (2003);  54 1-10
• 10 Ault J. G., Nicklas R. B.. Tension, microtubule rearrangements, and the proper distribution of chromosomes in mitosis.  Chromosoma. (1989);  98 33-39
• 11 Azumi Y., Liu D., Zhao D., Li W., Wang G., Hu Y., Ma H.. Homologue interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein.  EMBO Journal. (2002);  21 3081-3095
• 12 Bahler J., Wyler T., Loidl J., Kohli J.. Unusual nuclear structures in meiotic prophase of fission yeast: A cytological analysis.  Journal of Cell Biology. (1993);  121 241-256
• 13 Bai X., Peirson B. N., Dong F., Xue C., Makaroff C. A.. Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. .  Plant Cell. (1999);  11 417-430
• 14 Barnes T. M., Kohara Y., Coulson A., Hekimi S.. Meiotic recombination, noncoding DNA and genomic organisation in Caenorhabditis elegans. .  Genetics. (1995);  141 159-179
• 15 Bass H. W., Marshall W. F., Sedat J. W., Agard D. A., Cande W. Z.. Telomeres cluster de novo before the initiation of synapsis; a 3-dimensional spatial analysis of telomere positions before and during meiotic prophase.  Journal of Cell Biology. (1997);  137 5-18
• 16 Bass H. W., Riera-Lizarazu O., Ananiev E. V., Bordoli S. J., Rines H. W., Phillips R. L., Sedat J. W., Agard D. A., Cande W. Z.. Evidence for the coincident initiation of homolog pairing and synapsis during the telomere-clustering (bouquet) stage of meiotic prophase.  Journal of Cell Science. (2000);  113 1033-1042
• 17 Baudat F., Nicolas A.. Clustering of meiotic double-strand breaks on yeast chromosome III.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 5213-5218
• 18 Bell G.. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkeley, CA; University of California Press (1982)
• 19 Bennett M. D., Smith J. B.. The effect of polyploidy on meiotic duration and pollen development in cereal anthers.  Proceedings of the Royal Society of London Series B. (1972);  181 81-107
• 20 Bhatt A. M., Lister C., Page T., Fransz P., Findlay K., Jones G. H., Dickinson H. G., Dean C.. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family.  Plant Journal. (1999);  19 463-472
• 21 Bhatt A. M., Canales C., Dickinson H. G.. Plant meiosis: the means to 1 N.  Trends in Plant Science. (2001);  6 114-121
• 22 Bishop D., Park D., Xu L., Kleckner N.. DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation and cell cycle progression.  Cell. (1992);  69 439-456
• 23 Blat Y., Protacio R. U., Hunter N., Kleckner N.. Physical and functional interactions among basic chromosome organisational features govern early steps of meiotic chiasma formation.  Cell. (2002);  111 791-802
• 24 Borde V., Goldman A. S. H., Lichten M.. Direct coupling between meiotic DNA replication and recombination initiation.  Science. (2000);  290 806-809
• 25 Bullard S. A., Kim S., Galbraith A. M., Malone R. E.. Double-strand breaks at the HIS2 recombination hot spot in Saccharomyces cerevisiae. .  Proceedings of the National Academy of Sciences of the USA. (1996);  93 13054-13059
• 26 Bundock P., Hooykaas P.. Severe developmental defects, hypersensitivity to DNA-damaging agents, and lengthened telomeres in Arabidopsis MRE11 mutants.  Plant Cell. (2002);  14 2451-2462
• 27 Cai X., Makaroff C. A.. The dsy10 mutation of Arabidopsis results in desynapsis and a general breakdown in meiosis.  Sexual Plant Reproduction. (2001);  14 63-67
• 28 Cao L., Alani E., Kleckner N.. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. .  Cell. (1990);  61 1089-1101
• 29 Carlson P. S.. Mitotic crossing-over in a higher plant.  Genetical Research in Cambridge. (1974);  24 109-122
• 30 Carlton P. M., Cowan C. R., Cande W. Z.. Directed motion of telomeres in the formation of the meiotic bouquet revealed by time course and simulation analysis.  Molecular Biology of the Cell. (2003);  14 2832-2843
• 31 Caryl A. P., Armstrong S. J., Jones G. H., Franklin F. C. H.. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. .  Chromosoma. (2000);  109 62-71
• 32 Caryl A. P., Jones G. H., Franklin F. C. H.. Dissecting plant meiosis using Arabidopsis thaliana mutants.  Journal of Experimental Botany. (2003);  54 25-38
• 33 Cavalier-Smith T.. Origins of the machinery of recombination and sex.  Heredity. (2002);  88 125-141
• 34 Chan A., Cande W. Z.. Maize meiotic spindles assemble around chromatin and do not require paired chromosomes.  Journal of Cell Science. (1998);  111 3507-3515
• 35 Chandley A. C., Bateman A. J.. Timing of spermatogenesis in Drosophila melanogaster using tritiated thymidine.  Nature. (1962);  193 299-300
• 36 Chaudhury A. M., Lavithis M., Taylor P. E., Craig S., Singh M. B., Signer E. R., Knox R. B., Dennis E. S.. Genetic control of male fertility in Arabidopsis thaliana: structural analysis of premeiotic developmental mutants.  Sexual Plant Reproduction. (1994);  7 17-28
• 37 Chen C., Marcus A., Li W., Hu Y., Vielle Calzada J.-P., Grossniklaus U., Cyr R. J., Ma H.. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis.  Development. (2002);  129 2401-2409
• 38 Civardi L., Xia T., Edwards K. J., Schnable P. S., Nikolau B. J.. The relationship between genetic and physical distances in the cloned a1-sh2 interval of Zea mays L. genome.  Proceedings of the National Academy of Sciences of the USA. (1994);  91 8268-8272
• 39 Cleveland L. R.. The origin and evolution of meiosis.  Science. (1947);  105 287-289
• 40 Cliften P., Sudarsanam P., Desikan A., Fulton L., Fulton B., Majors J., Waterston R., Cohen B. A., Johnston M.. Finding functional features in Saccharomyces genomes by phylogenetic footprinting.  Science. (2003);  301 71-76
• 41 Cohen P. E., Pollard J. W.. Regulation of meiotic recombination and prophase I progression in mammals.  BioEssays. (2001);  23 996-1009
• 42 Copenhaver G. P., Browne W. E., Preuss D.. Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads.  Proceedings of the National Academy of Sciences of the USA. (1998);  95 247-252
• 43 Couteau F., Belzile F., Horlow C., Grandjean O., Vezon D., Doutriaux M. P.. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. .  Plant Cell. (1999);  11 1623-1634
• 44 Das O. P., Levi-Minzi S., Koury M., Benner M., Messing J.. A somatic gene rearrangement contributing to genetic diversity in maize.  Proceedings of the National Academy of Sciences of the USA. (1990);  87 7809-7813
• 45 Davis L., Smith G. R.. Meiotic recombination and chromosome segregation in Schizosaccharomyces pombe. .  Proceedings of the National Academy of Sciences of the USA. (2001);  98 8395-8402
• 46 Dawe R. K.. Meiotic chromosome organization and segregation in plants.  Annual Review of Plant Physiology and Plant Molecular Biology. (1998);  49 371-395
• 47 Dawkins R.. The Extended Phenotype. Oxford; Oxford University Press (1982)
• 49 Dernburg A. F., Sedat J. W., Cande W. Z., Bass H. W.. Cytology of telomeres. Blackburn, E. H. and Grieder, C. W., eds. Telomeres . Cold Spring Harbor, New York; Cold Spring Harbor Laboratory Press (1995): 295-337
• 50 Dernburg A. F., McDonald K., Moulder G., Barstead R., Dresser M., Villeneuve A. M.. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis.  Cell. (1998);  94 387-398
• 51 de Rooij D. G.. Proliferation and differentiation of spermatogonial stem cells.  Reproduction. (2001);  121 347-354
• 52 Dickinson H.. The regulation of alternation of generation in flowering plants.  Biological Reviews of the Cambridge Philosphical Society. (1994);  69 419-422
• 53 Dresser M. E.. Chromosome behaviour in Saccharomyces cerevisiae and (mostly) mammals.  Mutation Research. (2000);  451 107-127
• 54 Edelmann W., Cohen P. E., Kane M., Lau K., Morrow B., Bennett S., Umar A., Kunkel T., Cattoretti G., Chaganti R.. et al. . Meiotic pachytene arrest in MLH1-deficient mice.  Cell. (1996);  85 1125-1134
• 55 Egel-Mitani M., Olson L. W., Egel R.. Meiosis in Aspergillus nidulans; another example for lacking synaptonemal complexes in the absence of crossover interference.  Hereditas. (1982);  97 179-187
• 56 Eijpe M., Heyting C., Gross B., Jessberger R.. Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes.  Journal of Cell Science. (2000);  113 673-682
• 57 Farmer J. B., Moore J. E. S.. The maiotic (sic) phase in animals and plants.  Quarterly Journal of Microscopical Science. (1905);  48 489-557
• 58 Forsburg S. L.. Only connect: Linking meiotic DNA replication to chromosome dynamics.  Molecular Cell. (2002);  9 703-711
• 59 Franklin A. E., McElver J., Sunjevaric I., Rothstein R., Bowen B., Cande W. Z.. Three-dimensional microscopy of the Rad51 recombination protein during meiotic prophase.  Plant Cell. (1999);  11 809-824
• 60 Fransz P., Armstrong S., Alonso-Blanco C., Fischer T. C., Torres-Ruiz R. A., Jones nal G. H.. Cytogenetics for the model system Arabidopsis thaliana. .  Plant Journal. (1998);  13 867-876
• 61 Gallego M. E., Jeanneau M., Granier F., Bouchez D., Bechtold N., White C. I.. Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity.  Plant Journal. (2001);  25 31-41
• 62 Garcia V., Bruchet H., Camescasse D., Granier F., Bouchez D., Tissier A.. AtATM is essential for meiosis and the somatic response to DNA damage in plants.  Plant Cell. (2003);  15 119-132
• 63 Gilbertson L. A., Stahl F. W.. A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. .  Genetics. (1996);  144 27-41
• 64 Gill K. S., Gill B. S., Endo T. R., Boyko E. V.. Identification and high-density mapping of gene-rich regions in chromosome group 5 of wheat.  Genetics. (1996);  143 1011-1012
• 65 Glover J., Grelon M., Craig S., Chaudhury A., Dennis E.. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis.  Plant Journal. (1998);  15 345-356
• 66 Goedecke W., Eijpe M., Offenberg H. H., van Aalderen M., Heyting C.. MRE11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis.  Nature Genetics. (1999);  23 194-198
• 67 Goldway M., Sherman A., Zenvirth D., Arbel T., Simchen G.. A short chromosomal region with major roles in yeast chromosome III meiotic disjunction, recombination and double-strand breaks.  Genetics. (1993);  133 159-169
• 68 Golubovskaya I. N.. Genetic control of meiosis.  International Review of Cytology. (1979);  58 247-290
• 69 Gottschalk W., Klein H. D.. The influence of mutated genes on sporogenesis. A survey of the genetic control of meiosis in Pisum sativum. .  Theoretical and Applied Genetics. (1976);  48 23-24
• 70 Goyon C., Lichten M.. Timing of molecular events in meiosis in Saccharomyces cerevisiae: Stable heteroduplex DNA is formed late in meiotic prophase.  Molecular and Cellular Biology. (1993);  13 373-382
• 71 Grelon M., Vezon D., Gendrot G., Pelletier G.. ATSPO11-1 is necessary for efficient meiotic recombination in plants.  EMBO Journal. (2001);  20 589-600
• 72 Grelon M., Gendrot G., Vezon D., Pelletier G.. The Arabidopsis MEI1 gene encodes a protein with five BRCT domains that is involved in meiosis-specific DNA repair events independent of SPO11-induced DSBs.  Plant Journal. (2003);  35 465-475
• 73 Haber J. E.. DNA recombination: the replication connection.  Trends in Biochemical Sciences. (1999);  24 271-275
• 74 Handel M. A., Cobb J., Eaker S.. What are the spermatocyte's requirements for successful meiotic division?.  Journal of Experimental Zoology. (1999);  285 243-250
• 75 Harrison B. J., Carpenter R.. Somatic crossing-over in Antirrhinum majus. .  Heredity. (1977);  38 169-189
• 76 Hartung F., Puchta H.. Isolation of the complete cDNA of the Mre11 homologue of Arabidopsis (accession No. AJ243822) indicates conservation of DNA recombination mechanisms between plants and other eukaryotes.  Plant Physiology. (1999);  121 312
• 77 Hartung F., Puchta H.. Molecular characterization of two paralogous SPO11 homologues in Arabidopsis thaliana. .  Nucleic Acids Research. (2000);  28 1548-1554
• 78 Hassold T., Hunt P.. To err (meiotically) is human: the genesis of human aneuploidy.  Nature Reviews in Genetics. (2001);  2 280-291
• 79 Hassold T., Merrill M., Adkins K., Freeman S., Sherman S.. Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16.  American Journal of Human Genetics. (1995);  57 867-874
• 80 Havekes F. W. J., de Jong J. H., Heyting C.. Comparative analysis of female and male meiosis in three meiotic mutants of tomato.  Genome. (1997);  40 879-886
• 81 Hawley R. S., Arbel T.. Yeast genetics and the fall of the classical view of meiosis.  Cell. (1993);  72 301-303
• 82 Hawley R. S., Theurkauf W. E.. Requiem for distributive segregation: achiasmate segregation in Drosophila females.  Trends in Genetics. (1993);  9 310-317
• 83 He C., Mascarenhas J. P.. MEI1, an Arabidopsis gene required for male meiosis: isolation and characterization.  Sexual Plant Reproduction. (1998);  11 199-207
• 84 Heller C. G., Clermont Y.. Spermatogenesis in man: an estimate of its duration.  Science. (1963);  140 184-186
• 85 Heslop-Harrison J. S.. The molecular cytogenetics of plants.  Journal of Cell Science. (1991);  100 15-21
• 86 Heyting C.. Synaptonemal complexes: Structure and function.  Current Opinion in Cell Biology. (1996);  8 389-396
• 87 Heyting C., Dietrich A. J. J., de Jong J. H., Hartsuiker E.. Immunocytochemical techniques applied to meiotic chromosomes. Gosden, J. R. Methods in Molecular Biology, Vol. 29: Chromosome Analysis Protocols. Totowa, NJ; Humana Press Inc. (1994): 287-301
• 88 Hillers K. J., Villeneuve A. M.. Chromosome-wide control of meiotic crossing over in C. elegans. .  Current Biology. (2003);  13 1641-1647
• 89 Hülskamp M., Parekh N. S., Grini P., Schneitz K., Zimmermann I., Lolle S. J., Pruitt R. E.. The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. .  Developmental Biology. (1997);  187 114-124
• 90 Irniger S., Piatti S., Michaelis C., Nasmyth K.. Genes involved in sister chromatid separation are needed for B-type cycling proteolysis in budding yeast.  Cell. (1995);  81 269-278
• 91 Jang J. K., Sherizen D. E., Bhagat R., Manheim E. A., McKim K. S.. Relationship of DNA double-strand breaks to synapsis in Drosophila. .  Journal of Cell Science. (2003);  116 3069-3077
• 92 Kaul M. L. H., Murthy T. G. K.. Mutant genes affecting higher plant meiosis.  Theoretical and Applied Genetics. (1985);  70 449-466
• 93 Kee K., Keeney S.. Functional interactions between Spo11 and REC102 during initiation of meiotic recombination in Saccharomyces cerevisiae. .  Genetics. (2002);  160 111-122
• 94 Keeney S.. The mechanism and control of meiotic recombination initiation.  Current Topics in Developmental Biology. (2001);  52 1-53
• 95 Klapholz S., Waddell C. S., Esposito R. E.. The role of the Spo11 gene in meiotic recombination in yeast.  Genetics. (1985);  110 187-216
• 96 Kleckner N.. Meiosis: how could it work?.  Proceedings of the National Academy of Sciences of the USA. (1996);  93 8167-8174
• 98 Klein S., Zenvirth D., Dror V., Barton A. B., Kaback D. B., Simchen G.. Patterns of meiotic double-strand breakage on native and artificial yeast chromosomes.  Chromosoma. (1996);  105 276-284
• 99 Klein F., Mahr P., Galova M., Buonomo S. C., Michaelis C., Nairz K., Nasmyth K.. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.  Cell. (1999);  98 91-103
• 100 Klimyuk V. I., Jones J. D. G.. AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression.  Plant Journal. (1997);  11 1-14
• 101 Koduro P. R. K., Rao M. K.. Cytogenetics of synaptic mutants in higher plants.  Theoretical and Applied Genetics. (1981);  59 197-214
• 102 Kohli J., Bahler J.. Homologous recombination in fission yeast: Absence of crossover interference and synaptonemal complex.  Experientia. (1994);  50 295-306
• 103 Koltunow A. M., Truettner J., Cox K. H., Wallroth M., Goldberg R. B.. Different temporal and spatial gene expression patterns occur during anther development.  Plant Cell. (1990);  2 1201-1224
• 104 Koren A., Ben-Aroya S., Kupiec M.. Control of meiotic recombination initiation: a role for the environment?.  Current Genetics. (2002);  42 129-139
• 105 Krausz C., Forti G., McElreavey K.. The Y chromosome and male fertility and infertility.  International Journal of Andrology. (2003);  2 70-75
• 106 Lambie E. J., Roeder G. S.. A yeast centromere acts in cis to inhibit meiotic gene conversion of adjacent sequences.  Cell. (1988);  52 863-873
• 107 Lichten M.. Meiotic recombination: Breaking the genome to save it.  Current Biology. (2001);  11 253-256
• 108 Lichten M., Goldman A. S. H.. Meiotic recombination hotspots.  Annual Review of Genetics. (1995);  29 423-444
• 109 Lebel E. G., Masson J., Bogucki A., Paszkowski J.. Stress-induced intrachromosomal recombination in plant somatic cells.  Proceedings of the National Academy of Sciences of the USA. (1993);  90 422-426
• 110 Lee B., Amon A.. Meiosis: How to create a specialized cell cycle.  Current Opinion in Cell Biology. (2001);  13 770-777
• 111 Lee J., Iwai T., Yokota T., Yamashita M.. Temporally and spatially selective loss of Rec8 protein from meiotic chromosomes during mammalian meiosis.  Journal of Cell Science. (2003);  116 2781-2790
• 112 LeMaire-Adkins R., Radke K., Hunt P. A.. Lack of checkpoint control at the metaphase/anaphase transition: a mechanism of meiotic nondisjunction in mammalian females.  Journal of Cell Biology. (1997);  139 1611-1619
• 113 Loidl J.. The initiation of meiotic chromosome pairing: The cytological view.  Genome. (1990);  33 759-778
• 114 Loidl J., Klein F., Scherthan H.. Homologous pairing is reduced but not abolished in asynaptic mutants of yeast.  Journal of Cell Biology. (1994);  125 1191-1200
• 115 Lydall D., Nikolsky Y., Bishop D. K., Weinert T.. A meiotic recombination checkpoint controlled by mitotic checkpoint genes.  Nature. (1996);  383 840-843
• 116 Lynn A., Koehler K. E., Judis L., Chan E. R., Cherry J. P., Schwartz S., Seftel A., Hunt P. A., Hassold T. J.. Covariation of synaptonemal complex length and mammalian meiotic exchange rates.  Science. (2002);  296 2222-2225
• 117 Maestra B., de Jong J. H., Shepherd K., Naranjo T.. Chromosome arrangement and behaviour of the two rye homologous telosomes at the onset of meiosis in disomic wheat 5RL addition lines with and without the Ph1 locus.  Chromosome Research. (2002);  10 655-667
• 118 Magnard J.-L., Yang M., Chen Y.-C. S., Leary M., McCormick S.. The Arabidopsis gene TARDY ASYNCHRONOUS MEIOSIS is required for the normal pace and synchrony of cell division during male meiosis.  Plant Physiology. (2001);  127 11731-11735
• 119 Mahadevaiah S. K., Turner J. M., Baudat F., Rogakou E. P., de Boer P., Blanco-Rodriguez J., Jasin M., Keeney S., Bonner W. M., Burgoyne P. S.. Recombinational DNA double-strand breaks in mice precede synapsis.  Nature Genetics. (2001);  27 271-276
• 120 Margulis L., Sagan D.. Origins of Sex. New Haven; Yale University Press (1986)
• 121 Martinez-Perez E., Shaw P., Moore G.. Polyploidy induces centromere association.  Journal of Cell Biology. (2000);  148 233-238
• 122 Martinez-Perez E., Shaw P., Moore G.. The Ph1 locus is needed to ensure specific somatic and meiotic centromere association.  Nature. (2001);  411 204-207
• 123 Masson J. E., Paszkowski J.. Arabidopsis thaliana mutants altered in homologous recombination.  Proceedings of the National Academy of Sciences of the USA. (1997);  94 11731-11735
• 124 Masterton J.. Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms.  Science. (1994);  264 421-423
• 125 Maynard Smith J., Szathmary E.. The Major Transitions in Evolution. New York; Freeman (1995)
• 126 McKim K. S., Green-Marroquin B. L., Sekelsky J. J., Chin G., Steinberg C., Khodosh R., Hawley R. S.. Meiotic synapsis in the absence of recombination.  Science. (1998);  279 876-878
• 127 McKim K. S., Hawley R. S.. Chromosomal control of meiotic cell division.  Science. (1995);  270 1595-1601
• 128 Mercier R., Grelon M., Vezon D., Horlow C., Pelletier G.. How to characterize meiotic functions in plants?.  Biochimie. (2001 a);  83 1023-1028
• 129 Mercier R., Vezon D., Bullier E., Motamayor J. C., Sellier A., Lefèvre F., Pelletier G., Horlow C.. Switch1 (Swi1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis.  Genes and Development. (2001 b);  15 1859-1871
• 130 Mercier R., Armstrong S. J., Horlow C., Jackson N. P., Makaroff C. A., Vezon D., Pelletier G., Jones G. H., Franklin F. C. H.. The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. .  Development. (2003);  130 3309-3318
• 131 Miyazaki W. Y., Orr-Weaver T. L.. Sister-chromatid cohesion in mitosis and meiosis.  Annual Review of Genetics. (1994);  28 167-187
• 132 Moens P. B., Kolas N. K., Tarsounas M., Marcon E., Cohen P. E., Spyropoulos B.. The time course and chromosomal localization of recombination-related proteins at meiosis in the mouse are compatible with models that can resolve the early DNA-DNA interactions without reciprocal recombination.  Journal of Cell Science. (2002);  115 1611-1622
• 133 Moore D. P., Orr-Weaver T. L.. Chromosome segregation during meiosis: building an unambivalent bivalent. Handel, M. A., ed. Meiosis and Gametogenesis. London; Academic Press (1998): 263-299
• 134 Moore D. P., Page A. W., Tang T. T., Kerrebrock A. W., Orr-Weaver T. L.. The cohesion protein MEI-S332 localises to condensed meiotic and mitotic centromeres until sister chromatids separate.  Journal of Cell Biology. (1998);  140 1003-1012
• 135 Moreau P. J. F., Zicker D., Leblon G.. One class of mutants with disturbed centromere cleavage and chromosome pairing in Sordaria macrospora. .  Molecular and General Genetics. (1985);  198 189-197
• 136 Motamayor J. C., Vezon D., Bajon C., Sauvanet A., Grandjean O., Marchand M., Berchtold N., Pelletier G., Horlow C.. Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch.  Sexual Plant Reproduction. (2000);  12 209-218
• 137 Muller H. J.. The mechanism of crossing over.  American Naturalist. (1916);  50 193-221 284-305 350-366 421-434
• 138 Nag D. K., Petes T. D.. Physical detection of heteroduplexes during meiotic recombination in the yeast Saccharomyces cerevisiae. .  Molecular and Cellular Biology. (1993);  13 2324-2331
• 139 Nag D. K., Scherthan H., Rockmill B., Bhargava J., Roeder G. S.. Heteroduplex formation and homolog pairing in yeast meiotic mutants.  Genetics. (1995);  141 75-86
• 140 Nasmyth K.. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis.  Annual Review of Genetics. (2001);  35 673-745
• 141 Nicklas R. B., Ward S. C., Gorbsky G. J.. Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint.  Journal of Cell Biology. (1995);  130 929-939
• 142 Oakberg E. F.. Duration of the spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium.  American Journal of Anatomy. (1956);  99 998-1002
• 143 Orr-Weaver T. L.. Meiosis in Drosophila: seeing is believing.  Proceedings of the National Academy of Sciences of the USA. (1995);  92 10443-10449
• 144 Padmore R., Cao L., Kleckner N.. Temporal comparison of recombination and synaptonemal complex formation during meiosis in Saccharomyces cerevisiae. .  Cell. (1991);  66 1239-1256
• 145 Page S. L., Hawley R. S.. Chromosome choreography: The meiotic ballet.  Science. (2003);  301 785-789
• 146 Paques F., Haber J. E.. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae.  Microbiology and Molecular Biology Reviews. (1999);  63 349-404
• 147 Pawlowski W. P., Golubovskaya I. N., Cande W. Z.. Altered nuclear distribution of recombination protein RAD51 in maize mutants suggests the involvement of RAD51 in meiotic homology recognition.  Plant Cell. (2003);  15 1807-1816
• 148 Pawlowski W. P., Golubovskaya I. N., Timofejeva L., Meeley R. B., Sheridan W. F., Cande W. Z.. Coordination of meiotic recombination, pairing, and synapsis by PHS1.  Science. (2004);  303 89-92
• 149 Pecina A., Smith K. N., Mézard C., Murakami H., Ohta K., Nicolas A.. Targeted stimulation of meiotic recombination.  Cell. (2002);  111 173-184
• 150 Peters J. L., Cnudde F., Gerats T.. Forward genetics and map-based cloning approaches.  Trends in Plant Science. (2003);  8 484-491
• 151 Petes T. D.. Meiotic recombination hot spots and cold spots.  Nature Reviews in Genetics. (2001);  2 360-369
• 152 Petronczki M., Siomos M. F., Nasmyth K.. Un ménage à quatre: The molecular biology of chromosome segregation in meiosis.  Cell. (2003);  112 423-440
• 153 Porceddu A., Reale L., Lanfaloni L., Moretti C., Sorbolini S., Tedeschini E., Ferranti F., Pezzotti M.. Cloning and expression analysis of a Petunia hybrida flower specific mitotic-like cyclin.  FEBS Letters. (1999);  462 211-215
• 154 Porter S. E., White M. A., Petes T. D.. Genetic evidence that the meiotic recombination hotspot at the HIS4 locus of Saccharomyces cerevisiae does not represent a site for a symmetrically processed double-strand break.  Genetics. (1993);  134 5-19
• 155 Preuss S. B., Britt A. B.. A DNA-damage-induced cell cycle checkpoint in Arabidopsis. .  Genetics. (2003);  164 323-334
• 156 Preuss D., Rhee S. Y., Davis R. W.. Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes.  Science. (1994);  264 1458-1460
• 157 Prieto I., Suja J. A., Pezzi N., Kremer L., Martinez-A. C., Rufas J. S., Barbero J. L.. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I.  Nature Cell Biology. (2001);  3 761-766
• 158 Puchta H., Hohn B.. From centimorgans to basepairs: homologous recombination in plants.  Trends in Plant Science. (1996);  1 340-348
• 159 Puchta H., Swoboda P., Hohn B.. Induction of intrachromosomal recombination in whole plants.  Plant Journal. (1995);  7 203-210
• 160 Quevedo C., Del Cerro A. L., Santos J. L., Jones G. H.. Correlated variation of chiasma frequency and synaptonemal complex length in Locusta migratoria. .  Heredity. (1997);  78 515-519
• 161 Rabitsch K. P., Petronczki M., Javerzat J.-P., Genier S., Chwalla B., Schleiffer A., Tanaka T. U., Nasmyth K.. Kinetochore recruitment of two nucleolar proteins is required for homolog separation in meiosis I.  Developmental Cell. (2003);  4 535-548
• 162 Rajewsky M. F., Engelbergs J., Thomale J., Schweer T.. Relevance of DNA repair to carcinogenesis and cancer therapy.  Recent Results in Cancer Research. (1998);  154 127-146
• 163 Reddy T. V., Kaur J., Agashe B., Sundaresan V., Siddiqi I.. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein.  Development. (2003);  130 5975-5987
• 164 Reinke V., Smith H. E., Nance J., Wang J., van Doren C., Begley R., Jones S. J. M., Davis E. B., Scherer S., Ward S., Kim S. K.. A global profile of germline gene expression in C. elegans. .  Molecular Cell. (2000);  6 605-616
• 165 Revenkova E., Eijpe M., Heyting C., Gross B., Jessberger R.. Novel meiosis-specific isoform of mammalian SMC1.  Molecular and Cellular Biology. (2001);  21 6984-6998
• 166 Rice W. R., Chippindale A. K.. Sexual recombination and the power of natural selection.  Science. (2001);  294 555-559
• 167 Riggs C. D.. Meiotin-1: the meiosis readiness factor?.  BioEssays. (1997);  19 925-931
• 168 Rockmill B., Fung J. C., Branda S. S., Roeder G. S.. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over.  Current Biology. (2003);  13 1954-1962
• 169 Roeder G. S.. Sex and the single cell: Meiosis in yeast.  Proceedings of the National Academy of Sciences of the USA. (1995);  92 10450-10456
• 170 Roeder G. S.. Meiotic chromosomes: it takes two to tango.  Genes and Development. (1997);  11 2600-2621
• 171 Roeder G. S., Bailis J. M.. The pachytene checkpoint.  Trends in Genetics. (2000);  16 395-398
• 172 Ross K. J., Fransz F., Jones G. H.. A light microscopic atlas of meiosis in Arabidopsis thaliana. .  Chromosome Research. (1996);  4 507-516
• 173 Ross K. J., Fransz P., Armstrong S. J., Vizir I., Mulligan B., Franklin F. C. H., Jones G. H.. Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA transformed lines.  Chromosome Research. (1997);  5 551-559
• 174 Sanchez-Moran E., Armstrong S. J., Santos J. L., Franklin F. C. H., Jones G. H.. Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. .  Genetics. (2002);  162 1415-1422
• 175 Sanders P. M., Bui A. Q., Weterings K., McIntire K. N., Hsu Y.-C., Lee P. Y., Truong M. T., Beals T. P., Goldberg R. B.. Anther developmental defects in Arabidopsis thaliana male-sterile mutants.  Sexual Plant Reproduction. (1999);  11 297-322
• 176 SanMiguel P., Tikhonov A., Jin Y. K., Motchoulskaia N., Zakharov D., Melake-Berhan A., Springer P. S., Edwards K. J., Lee M., Avramova Z., Bennetzen J. L.. Nested retrotransposons in the intergenic regions of the maize genome.  Science. (1996);  274 765-768
• 177 Schedl T.. Developmental genetics of the germline. Riddle, D. L., Blumenthal, T., Meyer, B. J., and Priess, J. R., eds. C. elegans II. Cold Spring Harbor, New York; Cold Spring Harbor Laboratory Press (1997): 241-269
• 178 Scherthan H., Weich S., Schwegler H., Heyting C., Harle M., Cremer T.. Centromere and telomere movements during early meiotic prophase of mouse and men are associated with the onset of chromosome pairing.  Journal of Cell Biology. (1996);  134 1109-1125
• 179 Scherthan H.. A bouquet makes ends meet.  Nature Review of Molecular and Cellular Biology. (2001);  2 621-627
• 180 Schmidt R., West J., Love K., Lenehan Z., Lister C., Thompson H., Bouchez D., Dear C.. Physical map and organization of Arabidopsis thaliana chromosome 4.  Science. (1995);  270 480-483
• 181 Schommer C., Beven A., Lawrenson T., Shaw P., Sablowski R.. AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis.  Plant Journal. (2003);  36 1-11
• 182 Schwacha A., Kleckner N.. Identification of joint molecules that form frequently between homologs but rarely between sister chromatids during yeast meiosis.  Cell. (1994);  76 51-63
• 183 Schwacha A., Kleckner N.. Identification of double Holliday junctions as intermediates in meiotic recombination.  Cell. (1995);  83 783-791
• 184 Sears E. R.. Misdivision of univalents in common wheat.  Chromosoma. (1952);  4 535-550
• 185 Shaw P., Moore G.. Meiosis: vive la difference!.  Current Opinion in Plant Biology. (1998);  458-462
• 186 Sherman J. D., Stack S. M., Anderson L. K.. Two-dimensional spreads of synaptonemal complexes from Solanaceous plants. IV. Synaptic irregularities.  Genome. (1989);  32 743-753
• 187 Siddiqi I., Ganesh G., Grossniklaus U., Subbiah V.. The DYAD gene is required for progression through female meiosis in Arabidopsis. .  Development. (2000);  127 197-207
• 188 Siller S.. Sexual selection and maintenance of sex.  Nature. (2001);  411 689-692
• 189 Simchen G., Hugerat Y.. What determines whether chromosomes segregate reductionally or equationally in meiosis?.  BioEssays. (1993);  15 1-8
• 190 Singh R. J.. Plant Cytogenetics. Boca Raton, FL; CRC Press (1993): 391
• 191 Skibbens R. V., Corson L. B., Koshland D., Hieter P.. Ctf7 p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery.  Genes and Development. (1999);  13 307-319
• 192 Smyth D. R., Bowman J. L., Meyerowitz E. M.. Early flower development in Arabidopsis. .  Plant Cell. (1990);  2 755-767
• 193 Spielman M., Preuss D., Li F.-L., Browne W. E., Scott R. J., Dickinson H. G.. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. .  Development. (1997);  124 2625-2657
• 194 Straight A. F.. Cell cycle: checkpoint proteins and kinetochores.  Current Biology. (1997);  7 613-616
• 196 Stuart D., Wittenberg C.. CLB5 and CLB6 are required for premeiotic DNA replication and activation of the meiotic S/M checkpoint.  Genes and Development. (1998);  12 2698-2710
• 197 Suja J. A., Antonio C., Debec A., Rufas J. S.. Phosphorylated proteins are involved in sister chromatid arm cohesion during meiosis I.  Journal of Cell Science. (1999);  112 2957-2969
• 198 Sun H., Treco D., Schultes N. P., Szostak J. W.. Double-strand breaks at an initiation site for meiotic gene conversion.  Nature. (1989);  338 87-90
• 199 Sym M., Engebrecht J., Roeder G. S.. ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.  Cell. (1993);  72 365-378
• 200 Sym M., Roeder G. S.. Crossover interference is abolished in the absence of a synaptonemal complex protein.  Cell. (1994);  79 283-292
• 201 Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W.. The double-strand-break repair model for recombination.  Cell. (1983);  33 25-35
• 202 Tanksley S. D., Ganal M. W., Prince J. P., de Vincente M. C.. et al. . High density molecular linkage maps of the tomato and potato genomes.  Genetics. (1992);  132 1141-1160
• 203 Toth A., Ciosk R., Uhlmann F., Galova M., Schleiffer A., Nasmyth K.. Yeast cohesin complex requires a conserved protein, Eco1 p(Ctf7), to establish cohesion between sister chromatids during DNA replication.  Genes and Development. (1999);  13 320-333
• 204 Toth A., Rabitsch K. P., Galova M., Schleiffer A., Buonomo S. B. C., Nasmyth K.. Functional genomics identifies monopolin: A kinetochore protein required for segregation of homologs during meiosis I.  Cell. (2000);  103 1155-1168
• 205 Tovar J., Lichtenstein C.. Somatic and meiotic chromosomal recombination between inverted duplications in transgenic tobacco plants.  Plant Cell. (1992);  4 319-332
• 206 Trelles-Sticken E., Dresser M. E., Scherthan H.. Meiotic telomere protein Ndj1 p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing.  Journal of Cell Biology. (2000);  151 95-106
• 207 Tung K.-S., Hong E.-J. E., Roeder G. S.. The pachytene checkpoint prevents accumulation and phosphorylation of the meiosis-specific transcription factor Ndt80.  Proceedings of the National Academy of Sciences of the USA. (2000);  22 12187-12192
• 208 Van Beneden E.. Recherches sur la maturation de l'oeuf, la fecondation et la division cellulaire.  Archives of Biology. (1883);  4 265-640
• 209 van Heemst D., Heyting C.. Sister chromatid cohesion and recombination in meiosis.  Chromosoma. (2000);  109 10-26
• 210 van Veen J. E., Hawley R. S.. Meiosis: when even two is a crowd.  Current Biology. (2003);  13 831-833
• 211 Vergowen R. P. F. A., Jacobs S. G. M., Huiskamp R., Davids J. A. G., de Rooij D. G.. Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice.  Journal of Reproduction and Fertility. (1991);  93 233-243
• 212 Vig B. K.. Somatic crossing over in Glycine max (L.) Merril: effects of some inhibitors of DNA synthesis on the induction of somatic crossing over and point mutations.  Genetics. (1973);  73 583-596
• 213 Villeneuve A. M., Hillers K. J.. Whence Meiosis?.  Cell. (2001);  106 647-650
• 214 von Wettstein D., Rasmussen S. W., Holm P. B.. The synaptonemal complex in genetic segregation.  Annual Review of Genetics. (1984);  18 331-413
• 215 Vousden K. H.. p53: death star.  Cell. (2000);  103 691-694
• 216 Walker M. Y., Hawley R. S.. Hanging on to your homolog: the roles of pairing, synapsis and recombination in the maintenance of homolog adhesion.  Chromosoma,. (2000);  109 3-9
• 217 Watanabe Y., Nurse P.. Cohesin Rec8 is required for reductional chromosome segregation at meiosis.  Nature. (1999);  400 461-464
• 218 Watanabe Y., Yokobayashi S., Yamamoto M., Nurse P.. Pre-meiotic S phase is linked to reductional chromosome segregation and recombination.  Nature. (2001);  409 359-363
• 219 Weiner B. M., Kleckner N.. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast.  Cell. (1994);  77 977-991
• 220 Weismann A.. On the signification of the polar globules.  Nature. (1887);  36 607-609
• 221 Wu T.-C., Lichten M.. Meiosis-induced double-strand break sites determined by yeast chromatin structure.  Science. (1994);  263 515-518
• 222 Xu X., Hsia A.-P., Zhang L., Nikolau B. J., Schnable P. S.. Meiotic recombination break points resolve at high rates at the 5′ end of a maize coding sequence.  Plant Cell. (1995);  7 2151-2161
• 223 Yang M., Hu Y., Lodhi M., McCombie W. R., Ma H.. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 11416-11421
• 224 Yang M., Ma H.. Male meiotic spindle lengths in normal and mutant Arabidopsis cells.  Plant Physiology. (2001);  126 622-630
• 225 Yang M., McCormick S.. The Arabidopsis MEI1 gene likely encodes a protein with BRCT domains.  Sexual Plant Reproduction. (2002);  14 355-357
• 226 Yang W.-C., Sundaresan V.. Genetics of gametophyte biogenesis in Arabidopsis. .  Current Opinion in Plant Biology. (2000);  3 53-57
• 227 Yang C.-Y., Spielman M., Coles J. P., Li Y., Ghelani S., Bourdon V., Brown R. C., Lemmon B. E., Scott R. J., Dickinson H. G.. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. .  Plant Journal. (2003 a);  34 229-240
• 228 Yang X., Makaroff C. A., Ma H.. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis.  Plant Cell. (2003 b);  15 1281-1295
• 229 Zalevsky J., MacQueen A. J., Duffy J. B., Kemphues K. J., Villeneuve A. M.. Crossing over during Caenorhabditis elegans meiosis requires a conserved MutS-based pathway that is partially dispensable in budding yeast.  Genetics. (1999);  153 1271-1291
• 230 Zetka M., Rose A.. Mutant rec-1 eliminates the meiotic pattern of crossing over in Caenorhabditis elegans. .  Genetics. (1995);  141 1339-1349
• 231 Zickler D., Kleckner N.. The leptotene-zygotene transition of meiosis.  Annual Review of Genetics. (1998);  32 619-697
• 232 Zickler D., Kleckner N.. Meiotic chromosomes: integrating structure and function.  Annual Review of Genetics. (1999);  33 603-754

Editor: J. Raven