Mechanisms of Meiosis

Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech-ERL3559 CNRS
Bâtiment 7
INRA Centre de Versailles-Grignon
Route de St-Cyr (RD10)
78026 Versailles Cedex France

tél : +33 (0)1 30 83 30 00 - fax : +33 (0)1 30 83 33 19

Meiosis
Meiosis is an essential stage in the life cycle of sexually-reproducing organisms. Indeed, meiosis is the specialized cell division that reduces the number of chromosomes from two sets in the parent to one set in gametes, while fertilization restores the original chromosome number. Meiosis is also the stage of development when genetic recombination occurs, thus being the heart of Mendelian heredity.
While events occurring during meiosis have been precisely described, the underlying mechanisms remain largely unknown. Major questions remain unanswered as: Why and how is the recombination rate along the chromosomes controlled?  How are the formation and the distribution of the recombination events along the chromosomes? Why are the pericentromeric regions refractory to meiotic recombination events? What is the signal of interference? What is the role of the synaptonemal complex? Which actors are involved in the choice between the homologous chromosome or the sister chromatid to repair DNA double-strand breaks? How are the chromosomes and then the sister chromatids separated during the two meiotic divisions? How are the meiotic divisions regulated ?
Arabidopsis emerged as one of the prominent models in the field of meiosis notably because of the possibility to combine large-scale genetic studies and the wide range of molecular and cytological tools.
Our projects aim to elucidate comprehensively the mechanisms of meiosis. Thanks to dedicated genetic screens; we identify new key actors that we then characterize using a whole set of combined approaches: genetics, molecular biology, cytogenetics, biochemistry and genomics. Our work contributes to a better understanding of key biological mechanisms crucial during meiosis such as homologous recombination, cell cycle or chromosome segregation. Increasing our knowledge on meiosis, in addition to its intrinsic interest, would have also important implications for agriculture and medicine.

Can plants give up sex?

Plants producing 2n gametes and clonal seeds

Taming genetic recombination

Crossing over with Raphaël Mercier: the mechanics of meiosis

Mutations: A major discovery with mutant Arabidopsis: imitating apomixis

FANCM limits meiotic crossovers.

Chambon, A., West, A., Vezon, D., Horlow, C., De Muyt, A., Chelysheva, L., Ronceret, A., Darbyshire, A., Osman, K., Heckmann, S., Franklin, F. C. H., Grelon, M. (2018). Identification of ASYNAPTIC4, a Component of the Meiotic Chromosome Axis. Plant Physiology, 178(1), 233-246.

Capilla-Perez, L., Solier, V., Portemer, V., Chambon, A., Hurel, A., Guillebaux, A., Vezon, D., Cromer, L., Grelon, M., Mercier, R. (2018). The HEM Lines: A New Library of Homozygous Arabidopsis thaliana EMS Mutants and its Potential to Detect Meiotic Phenotypes. Frontiers in Plant Science, 9, 1339.

Fernandes JB, Duhamel M, Seguéla-Arnaud M, Froger N, Girard C, Choinard S, De Winne N, De Jaeger G, Gevaert K, Andrey P, Grelon M, Guerois R, Kumar R, Mercier R (2018) FIGL1 and its novel partner FLIP form a conserved complex that regulates homologous recombination. PLoS Genet. doi: 10.1371/journal.pgen.1007317

Hurel, A., Phillips, D., Vrielynck, N., Mézard, C., Grelon, M. and Christophorou, N. (2018) A cytological approach to studying meiotic recombination and chromosome dynamics in Arabidopsis thaliana male meiocytes in three dimensions. Plant J. 95:385-396.

Séguéla-Arnaud M, Choinard S, Larchevêque C, Girard C, Froger N, Crismani W, Mercier R (2017) RMI1 and TOP3a limit meiotic CO formation through their C-terminal domains. Nucleic Acids Res 45: 1860-1871

Fernandes JB, Seguéla-Arnaud M, Larchevêque C, Lloyd AH, Mercier R (2017) Unleashing meiotic crossovers in hybrid plants. Proc Natl Acad Sci U S A 115:2431-2436.

Séguéla-Arnaud M, Choinard S, Larchevêque C, Girard C, Froger N, Crismani W, Mercier R. (2016) RMI1 and TOP3a limit meiotic CO formation through their C-terminal domains. Nucleic Acids Res. Dec 13. pii: gkw1210. [Epub ahead of print] PMID: 27965412 (pdf)

Cifuentes, M., Jolivet, S., Cromer, L., et al. (2016) TDM1 Regulation Determines the Number of Meiotic Divisions. PLOS Genet., 12, e1005856. (pdf)

Vrielynck N, Chambon A, Vezon D, Pereira L, ChelyshevaL, De Muyt A, Mézard C, Mayer C, Grelon M. (2016). A DNA topoisomerase VI-like complex initiates meiotic recombination. Science.351(6276):939-43. doi: 10.1126/science.aad5196 (full text) communiqué de presse INRA

Mézard C, Tagliaro Jahns M, Grelon M (2015). Where to cross? New insights into the location of meiotic crossovers. Trends Genet 1–9 (pubmed)

Mercier R, Mézard C, Jenczewski E, Macaisne N, Grelon M. (2015). The Molecular Biology of Meiosis in Plants. Annu Rev Plant Biol 66: 297–327 (pubmed)

Girard, C., Chelysheva, L., Choinard, S., Froger, N., Macaisne, N., Lehmemdi, A., Mazel, J., Crismani, W. and Mercier, R. (2015) AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM Antagonize Meiotic Crossovers by Distinct Mechanisms M. Lichten, ed. PLOS Genet., 11, e1005369. (pdf)

Mercier, R., Mézard, C., Jenczewski, E., Macaisne, N. and Grelon, M. (2015) The molecular biology of meiosis in plants. Annu. Rev. Plant Biol., 66, 297–327.

Portemer, V., Renne, C., Guillebaux, A. and Mercier, R. (2015) Large genetic screens for gynogenesis and androgenesis haploid inducers in Arabidopsis thaliana failed to identify mutants. Front. Plant Sci., 6,1–6. (pdf)

Séguéla-Arnaud, M., Crismani, W., Larchevêque, C., et al. (2015) Multiple mechanisms limit meiotic crossovers: TOP3a and two BLM homologs antagonize crossovers in parallel to FANCM. Proc. Natl. Acad. Sci. U. S. A., 112, 4713–4718.

Duroc, Y., Lemhemdi, A., Larcheveque, C., Hurel, A., Cuacos, M., Cromer, L., Armstrong, S.J., Chelysheva, L. and Mercier, R. (2014) The kinesin AtPSS1 promotes synapsis and is required for proper crossover distribution in meiosis. PLoS Genet., 10, e1004674. (pdf)

Girard, C., Crismani, W., Froger, N., Mazel, J., Lemhemdi, A., Horlow, C. and Mercier, R. (2014) FANCM-associated proteins MHF1 and MHF2, but not the other Fanconi anemia factors, limit meiotic crossovers. Nucleic Acids Res., 42, 9087–9095.

Jahns MT, Vezon D, Chambon A, Pereira L, Falque M, Martin OC, Chelysheva L, Grelon M. (2014). Crossover localisation is regulated by the neddylation posttranslational regulatory pathway. PLoS Biol. Aug 12;12(8):e1001930. doi: 10.1371/journal.pbio.1001930. (online)

Jenczewski E, Mercier R, Macaisne N, and Mézard C. (2013). Meiosis: Recombination and the control of cell division. In: Plant Genome Diversity Volume 2: 121-136. Springer-Verlag. I.J. Leitch et al. (Eds)

Uanschou C, Ronceret A, Von Harder M, De Muyt A, Vezon D, Pereira L, Chelysheva L, Kobayashi W, Kurumizaka H, Schlögelhofer P, Grelon M. (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(12):4924-40. doi: 10.1105/tpc.113.118521. (pubmed)

Mézard C, Macaisne N, Grelon M (2013). La Méiose in La Reproduction Animale et Humaine. Editions Quae _ Éditions Cemagref, Cirad, Ifremer

Chelysheva L, Grandont L, Grelon M (2013). Immunolocalization of meiotic proteins in Brassicacae: method 1 in  Plant Meiosis (eds : Pawlowski W Grelon M and Armstrong S). Series: Methods in Molecular Biology (Series Editor: John M. Walker) 990:93-101. (pubmed)

Pawlowski, W.P.; Grelon, M; Armstrong, S (Eds.) (2013). Plant Meiosis, Methods and Protocols, Series: Methods in Molecular Biology, Vol. 990 XV, 238 p. 52 illus., 28 illus. in color. Humana Press

Drouaud, J, Khademian, J., Giraut, L., and Mézard, C. (2013). Contrasted patterns of crossover and non crossover events at Arabidopsis thaliana meiotic recombination hotspots. PLos Gentics DOI: 10.1371/journal.pgen.1003922 (online)

Cifuentes, M., Rivard, M., Pereira, L., Chelysheva, L. and Mercier, R. (2013) Haploid meiosis in Arabidopsis: double-strand breaks are formed and repaired but without synapsis and crossovers. PLoS One,8, e72431. (pdf)

Jenczewski, E., Mercier, R., Macaisne, N., and Mezard, C. (2013) Meiosis: Recombination and the Control of Cell Division, in Plant Genome Diversity Volume 2 (Greilhuber, J., Dolezel, J., and Wendel, J. F., Eds.), pp 121–136. Springer Vienna, Vienna

Crismani, W., and Mercier, R. (2013) Plant Meiosis, Plant Meiosis (Pawlowski, W. P., Grelon, M., and Armstrong, S., Eds.), pp 227–234. Humana Press, Totowa, NJ.

Crismani, W., Portemer, V., Froger, N., Chelysheva, L., Horlow, C., Vrielynck, N. and Mercier, R. (2013) MCM8 Is Required for a Pathway of Meiotic Double-Strand Break Repair Independent of DMC1 in Arabidopsis thaliana. PLoS Genet., 9, e1003165. (pdf)

Crismani, W., Girard, C., and Mercier, R. (2013) Tinkering with meiosis., Journal of experimental botany 64, 55–6

Crismani W, Mercier R (2012) What limits meiotic crossovers? Cell cycle (Georgetown, Tex) 11: 3527–3528.

Eloy NB, Gonzalez N, Van Leene J, Maleux K, Vanhaeren H, et al. (2012) SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. Proceedings of the National Academy of Sciences of the United States of America 109: 13853–13858.

Crismani W, Girard C, Froger N, Pradillo M, Santos JL, et al. (2012) FANCM limits meiotic crossovers. Science (New York, NY) 336: 1588–1590.

Cromer L, Heyman J, Touati S, Harashima H, Araou E, et al. (2012) OSD1 Promotes Meiotic Progression via APC/C Inhibition and Forms a Regulatory Network with TDM and CYCA1;2/TAM. PLoS genetics 8: e1002865. (pdf)

Yelina NE, Choi K, Chelysheva L, Macaulay M, De Snoo B, Wijnker E, Miller N, Drouaud J, Grelon M, Copenhaver GP, et al (2012). Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS genetics 8: e1002844 (online)

Chelysheva L, Vezon D, Chambon A, Gendrot G, Pereira L, Lemhemdi A, Vrielynck N, Le Guin S, Novatchkova M, Grelon M (2012). The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS genetics 8: e1002799 (online)

Giraut, L., Falque, M., Drouaud, J., Pereira, L., Martin, O.C., and Mézard, C. (2011). Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex specific patterns long chromosomes. PLos Gentics DOI: 10.1371/journal.pgen.1002354 (online)

Jenczewski, E., Mercier, R., Macaisne, N., and Mézard, C. (2011). Meiosis : recombination and the control of cell division. Plant génome diversity, ed. J. Greilhuber, J. Wendel, I.J. Leitch and J. Dolezel. Springer-Verlag Wien New York, submitted

Drouaud, J. and Mézard, C. Characterization of meiotic crossovers in pollen from Arabidopsis thaliana (2011). Methods Mol. Biol. 745:223-49. doi: 10.1007/978-1-61779-129-1_14. (pubmed)

Macaisne N, Vignard J, Mercier R*. SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers. J Cell Sci. 2011 15;124(Pt 16):2687-91.

Libeau P, Durandet M, Granier F, Marquis C, Berthomé R, Renou JP, Taconnat-Soubirou L, Horlow C. Gene expression profiling of Arabidopsis meiocytes.Plant Biol (Stuttg). 2011 Sep; 13(5):784-93

Marimuthu MP, Jolivet S, Ravi M, Pereira L, Davda JN, Cromer L, Wang L, Nogué F, Chan SW, Siddiqi I, Mercier R. Synthetic clonal reproduction through seeds. Science. 2011 Feb 18;331(6019):876.

Chelysheva L, Grandont L, Vrielynck N, le Guin S, Mercier R, Grelon M. (2010). An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis; immunodetecion of cohesins, histones and MLH1.Cytogenetics and Genome Research. 129:143-153

d'Erfurth, I., Cromer, L, Jolivet, S, Girard, C, Horlow, C, Sun, Y, To, JP, Berchowitz, LE, Copenhaver, GP, and Mercier, R*. The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet. 2010. e1000989. (pdf)

d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R*. Turning Meiosis into Mitosis. PLoS Biol 2009. 7(6): e1000124. (pdf)

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