Abstract
Inverted meiosis is observed in plants (Cyperaceae and Juncaceae) and insects (Coccoidea, Aphididae) with holocentric chromosomes, the centromeres of which occupy from 70 to 90% of the metaphase chromosome length. In the first meiotic division (meiosis I), chiasmata are formed and rodlike bivalents orient equationally, and in anaphase I, sister chromatids segregate to the poles; the diploid chromosome number is maintained. Non-sister chromatids of homologous chromosomes remain in contact during interkinesis and prophase II and segregate in anaphase II, forming haploid chromosome sets. The segregation of sister chromatids in meiosis I was demonstrated by example of three plant species that were heterozygous for chromosomal rearrangements. In these species, sister chromatids, marked with rearrangement, segregated in anaphase I. Using fluorescent antibodies, it was demonstrated that meiotic recombination enzymes Spo11 and Rad5l, typical of canonical meiosis, functioned at the meiotic prophase I of pollen mother cells of Luzula elegance and Rhynchospora pubera. Moreover, antibodies to synaptonemal complexes proteins ASY1 and ZYP1 were visualized as filamentous structures, pointing to probable formation of synaptonemal complexes. In L. elegance, chiasmata are formed by means of chromatin threads containing satellite DNA. According to the hypothesis of the author of this review, equational division of sister chromatids at meiosis I in the organisms with inverted meiosis can be explained by the absence of specific meiotic proteins (shugoshins). These proteins are able to protect cohesins of holocentric centromeres from hydrolysis by separases at meiosis I, as occurs in the organisms with monocentric chromosomes and canonical meiosis. The basic type of inverted meiosis was described in Coccoidea and Aphididae males. In their females, the variants of parthenogenesis were also observed. Until now, the methods of molecular cytogenetics were not applied for the analysis of inverted meiosis in Coccoidea and Aphididae. Evolutionary, inverted meiosis is thought to have appeared secondarily as an adaptation of the molecular mechanisms of canonical meiosis to chromosome holocentrism.
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Malheiros, N., Castro, D., and Câmara, A., Cromosomas sem centrómero localizado: o caso de Luzula purpurea Link., Agron. Lusit., 1947, vol. 9, pp. 51–73.
Hughes-Schraeder, S., Cytology of coccids (Coccoidea—Homoptera), Adv. Genet., 1948, vol. 2, pp. 127–203.
Rhoades, M.M., Meiosis, in The Cell, Brachet, J. and Mirsky, A.E., Eds., vol. 3: Mitosis and Meiosis, New York: Acad. Press, 1961, pp. 1–76.
John, B., Meiosis, Cambridge Cambridge Univ. Press, 1990.
Cabral, G., Marques, A., Schubert, V., et al., Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes, Nat. Commun., 2014. doi 10.1038/ncomms6070
Heckman, S., Jankowska, M., Schubert, V., et al., Alternative meiotic chromatid segregation in the holocentric plant Luzula elegans, Nat. Commun., 2014. doi 10.1038/ncomms5979
Li, W. and Zeng, G.-Ch., A resurgent phoenix—a hypothesis for the origin of meiosis, IUBMB Life, 2002, vol. 54, pp. 9–12. doi 10.1080/15216540290106413
Wilkins, A.S. and Holliday, R., The evolution of meiosis from mitosis, Genetics, 2009, vol. 181, pp. 3–12. doi 10.1534/genetics.108.099762
Marcon, E. and Moens, H.B., The evolution of meiosis: recruitment and modification of somatic DNArepair proteins, BioEssay, 2005, vol. 27, pp. 795–808.
Anuradha, S. and Muniyappa, K., Molecular aspects of meiotic chromosome synapsis and recombination, Prog. Nucl. Acid Res. Mol. Biol., 2005, vol. 79, pp. 49–132. doi 10.1016/S0079-6603(4)79002-9
Bogdanov, Yu.F., Grishaeva, T.M., and Dadashev, S.Ya., Similarity of the domain structure of proteins as a basis for the evolutionarily conservation of meiosis, Int. Rev. Cytol., 2007, vol. 257, pp. 83–142.
Egel, R. and Penny, D., On the origin of meiosis in eukaryotic evolution: coevolution of meiosis and mitosis from feeble beginnings, in Genome Dynamics and Stability, vol. 3: Recombination and Meiosis, Egel, R. and Lankenau, D.-H., Eds., Berlin: Springer-Verlag, 2007, pp. 249–288.
Grishaeva, T.M. and Bogdanov, Yu.F., Conservation and variability of synaptonemal complex proteins in phylogenesis of eukaryotes, Int. J. Evol. Biol., 2014, article ID 856230. doi 10.1155/2014/856230
Anderson, L.K., Offenberg, H.H., Verkuijilen, W.M.H.C., and Heyting, C., Rec-A-like proteins are components of the meiotic nodules in lily, Proc. Natl. Acad. Sci. U.S.A., 1997, vol. 94, pp. 6868–6973.
Trelles-Sticken, E., Dresse, M.E., and Scherthan, H., Meiotic telomere protein Ndj1 is required for meiosisspecific telomere distribution, bouquet formation and efficient homolog pairing, J. Cell Biol., 2000, vol. 151, p. 106.
Lichten, M., Meiotic recombination: breaking the genome to save it, Curr. Biol., 2001, vol. 11, pp. R253–R256.
Shinohara, A. and Shinohara, M., Roles of RecA homologues Rad51 and Dmc1 during meiotic recombination, Cytogen. Genome Res., 2004, vol. 107, pp. 201–207.
Börner, G.V., Kleckner, N. and Hunter, N., Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis, Cell, 2004, vol. 117, pp. 29–45.
Anderson, L.K., Royer, S.M., Page, S.L., et al., Juxtaposition of C(2)M and the transversal filament protein C(3)G within the central element of Drosophila synaptonemal complex, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, pp. 4482–4487.
Gerton, J. and Hawley, R.S., Homologous chromosome interactions in meiosis: diversity amidst conservation, Nat. Rev. Genet., 2005, vol. 6, pp. 477–487.
Zickler, D. and Kleckner, N., Recombination, pairing and synapsis of homologs during meiosis, Cold Spring Harbor Perspect. Biol., 2015, pp. 1–26. doi 10.110/cshperspecta016626
Grishaeva, T.M. and Bogdanov, Yu.F., Genetic control of meiosis in Drosophila, Russ. J. Genet., 2000, vol. 36, no. 10, pp. 1089–1106.
Golubovskaya, I.N., Hammer, O., Timofeeva, L.P., et al., Alleles of afd1 dissect REC8 functions during meiotic prophase I, J. Cell Sci., 2006, vol. 119, pp. 3306–3315.
Torgasheva, A.A., Rubtsov, N.B., and Borodin, P.M., Recombination and synaptic adjustment in oocytes of mice heterozygous for a large paracentric inversion, Chromosome Res., 2013, vol. 21, pp. 37–48.
Raikov, I.B., Meiosis in protists: recent advances and persisting problems, Eur. J. Protistol., 1995, vol. 31, pp. 1–7.
Seravin, D.N. and Gudkov, A.V., Agamnye sliyaniya protistov i proiskhozhdenie polovogo protsessa (Agamic Fusion of Protists and the Origin of Sexual Process), St. Petersburg, 1999.
Solari, A.J., Primitive forms of meiosis: the possible evolution of meiosis, Biocell, 2002, vol. 26, no. 1, pp. 1–13.
Cavalier-Smith, T., Origins of the machinery of recombination and sex, Heredity, 2000, vol. 88, pp. 125–141.
Bogdanov, Yu.F., Variation and evolution of meiosis, Russ. J. Genet., 2003, vol. 39, no. 4, pp. 369–381.
Bogdanov, Yu.F., Similarity of domain organization of proteins in phylogenetically distant organisms as a basis of meiosis conservatism, Russ. J. Dev. Biol., 2004, vol. 35, no. 6, pp. 337–345.
Bogdanov, Yu.F., Evolution of meiosis of unicellulate and multicellular eukaryotes: aromorphosis at the cellular level, Zh. Obshch. Biol., 2008, vol. 69, no. 2, pp. 102–117.
Grishaeva, T.M. and Bogdanov, Yu.F., On the origin of synaptonemal complex proteins: search for related proteins in proteomes of algae, lower fungi, mosses, and protozoa, Russ. J. Genet.: Appl. Res., 2013, vol. 3, no. 6, pp. 481–486.
Comings, D.E. and Okada, T., Holocentric chromosomes in Oncopeltus: kinetochore plates are present in mitosis but absent in meiosis, Chromosoma, 1972, vol. 37, pp. 177–192.
Rog, O. and Dernburg, A.E., Chromosome pairing and synapsis during Caenorhabditis elegans meiosis, Curr. Opin. Cell Biol., 2013, vol. 25, pp. 349–356.
Lui, D.Y., and Colaiacóvo, M.P., Meiotic development in Caenorhabditis elegans, Adv. Exp. Mol. Biol., 2013, vol. 757, pp. 133–170.
Rasmussen, S.W., The transformation of the synaptonemal complex into “elimination chromatin” in Bombyx mori oocytes, Chromosoma, 1977, vol. 60, pp. 205–221.
Rasmussen, S.W. and Holm, P.B., Chromosome pairing, recombination nodules, and chiasma formation in diploid Bombyx mori male, Carlsberg Res. Commun., 1980, vol. 45, pp. 483–548.
Traut, W., A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of Ephestia kuehniella (Lepidoptera), Genetics, 1977, vol. 47, pp. 135–142.
Kuznetsova, V.G. and Grozeva, S., Achiasmatic meiosis: a review, Inf. Vestn. Vavilovskogo O-va Genet. Sel., 2010, vol. 14, no. 1, pp. 79–88.
Nordenskiöld, H., Study of meiosis in Luzula purpurea, Hereditas, 1962, vol. 48, pp. 503–513.
Nordenskiöld, H., A study of meiosis in the progeny of X-irradiated Luzula purpurea, Hereditas, 1963, vol. 49, pp. 33–47.
Bongiorni, S., Florenzo, P., Pippoletti, D., and Prantera, G., Inverted meiosis and meiotic drive in mealybugs, Chromosoma, 2004, vol. 112, pp. 332–342. doi 10.1007/s00412-004-0278-4
Srinivasan, D.G., Fenton, B., Jaubert-Possamai, S., and Jaouannet, M., Analysis of meiosis and cell cycle genes of the facultatively asexual pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae), Insect. Mol. Biol., 2010, vol. 19, suppl. 2, pp. 229–239. doi 10.1111/j.1365–2583.2009.00960x. PMID: 20482653.
Srinivasan, D.G., Abdelhady, A., and Stern, D.L., Gene expression analysis of parthenogenetic embryonic development of the pea aphid, Acyrthosiphon pisum, suggests that aphid parthenogenesis evolved from meiotic oogenesis, PLoS One, 2014, vol. 9, no. 12. e115099. doi 10.1371/journalpone.0115099. eCollection 2014.
Grozeva, S., Nokkala, S., and Smirnov, N., First evidence of chromosome pre-reduction in male meiosis in the Miridae bugs (Heteroptera), Folia Boil. (Krakow.), 2006, vol. 54, pp. 9–12.
Viera, A., Page, J., and Rufas, J.S., Inverted meiosis: the true bugs as a model to study, in Genome Dynamics, Benavente, R. and Volff, J.-N., Eds., Basel: Karger, 2009, vol. 5, pp. 137–156.
Grishaeva, T.M., Kulichenko, D.A., and Bogdanov, Yu.F., Comparative conservatism of different shugoshin groups—chromatid cohesion protectors in eukaryotes: scientific review, in Proceedings of International Scientific Conference, (Karlovy Vary–Moscow, May 29–30, 2015), Karlovy Vary: Sklen ny -M stek, 2015, pp. 11–21.
Kitajima, T.S., Kawashima, S.A., and Watanabe, Y., The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis, Nature, 2004, vol. 427, pp. 510–517.
Watanabe, Y., Shugoshin: guardian spirit at the centromere, Curr. Opin. Cell Biol., 2005, vol. 17, pp. 590–595.
Peters, J.M., Tedeschi, A., and Schmitz, J., The cohesin complex and its roles in chromosome biology, Genes Dev., 2008, vol. 22, pp. 3089–3114.
Gutierrez-Caballero, C., Cebollero, L.R., and Pendas, A.M., Shugoshins: from protectors of cohesion to versatile adaptors at the centromere, Trends Genet., 2012, vol. 28, pp. 351–360.
Zamariola, L., De Storme, N., Vannerum, K., et al., SHUGOSHINs and PATRONUS protect meiotic centromere cohesion in Arabidopsis thaliana, Plant J., 2014, vol. 77, pp. 782–794.
Grishaeva, T.M., Dadashev, S.Ya., and Bogdanov, Yu.F., Meiotic Rec8 cohesins and their mitotic Rad21 orthologs: comparison in silico, Mol. Biol. (Moscow), 2007, vol. 41, no. 4, pp. 674–676.
Murrey, A.W. and Szostack, J.W., Chromosome segregation in mitosis and meiosis, Annu. Rev. Cell Biol., 1985, vol. 1, pp. 289–315.
Wrensch, D.L., Kethley, J.B., and Norton, R.A., Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes, in Mites: Ecological and Evolutionary Analyses of Life History Patterns, Houck, M.A., Ed., New York: Chapman and Hall, 1993, pp. 282–343.
Kolomiets, O.L., Atsaeva, M.M., Dadashev, S.Ya., S.K. Abilev, V.E. Spangenberg, and S.N. Matveevsky, Damage to synaptonemal complex structure and peculiarities of selection of mouse spermatocytes I at response to drug administration, Russ. J. Genet., 2013, vol. 49, no. 11, pp. 1098–1106.
Mikhailova, E.I., Lovtsyus, A.V., and Sosnikhina, S.P., Some features of meiosis key events in rye and its synaptic mutants, Russ. J. Genet., 2010, vol. 46, no. 10, pp. 1210–1213.
Simanovskii, S.A., Matveevskii, S.N., Iordanskaya, I.V., et al., Spiral cores of synaptonemal complex lateral elements at the diplotene stage in rye include the ASY1 protein, Russ. J. Genet., 2014, vol. 50, no. 10, pp. 1107–1111.
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Original Russian Text © Yu.F. Bogdanov, 2016, published in Genetika, 2016, Vol. 52, No. 5, pp. 541–560.
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Bogdanov, Y.F. Inverted meiosis and its place in the evolution of sexual reproduction pathways. Russ J Genet 52, 473–490 (2016). https://doi.org/10.1134/S1022795416050033
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DOI: https://doi.org/10.1134/S1022795416050033