Chiasmatic and achiasmatic inverted meiosis of plants with holocentric chromosomes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Cabral, Gabriela ^a,b   Marques, André ^a   Schubert, Veit ^c   Pedrosa Harand, Andrea ^a   Schlögelhofer, Peter ^b  

^a FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^b UNIVERSITY OF VIENNA   (Austria)

^c LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CHROMOSOME; DNA; SEDGE;

ARTICLE; CHROMOSOME; DIPLOIDY; HOLOCENTRIC CHROMOSOME; MEIOSIS; NONHUMAN; PLANT; PLANT GENOME; PROPHASE; RHYNCHOSPORA PUBERA; RHYNCHOSPORA TENUIS; SISTER CHROMATID; CENTROMERE; CHROMATIN; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CYPERACEAE; PHYSIOLOGY; PLANT CHROMOSOME;

RHYNCHOSPORA PUBERA;

CHROMATIN;

CENTROMERE; CHROMATIN; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; CHROMOSOMES, PLANT; CYPERACEAE; MEIOSIS;

EID: 84920594663     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6070     Document Type: Article

References (62)

1. Marston, A. L. Chromosome segregation in budding yeast: sister chromatid cohesion and related mechanisms. Genetics 196, 31-63 (2014).
2. McNicoll, F., Stevense, M., & Jessberger, R. Cohesin in gametogenesis. Curr. Top. Dev. Biol. 102, 1-34 (2013).
3. Keeney, S. Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn. Stab. 2, 81-123 (2008).
4. Keeney, S., & Neale, M. J. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523-525 (2006).
5. Edlinger, B., & Schlogelhofer, P. Have a break: determinants of meiotic DNA double strand break (DSB) formation and processing in plants. J. Exp. Bot. 62, 1545-1563 (2011).
6. Page, S. L., & Hawley, R. S. Chromosome choreography: the meiotic ballet. Science 301, 785-789 (2003).
7. de Boer, E., & Heyting, C. The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115, 220-234 (2006).
8. Hamant, O., Ma, H., & Cande, W. Z. Genetics of meiotic prophase I in plants. Annu. Rev. Plant Biol. 57, 267-302 (2006).
9. Hunter, N. in Molecular Genetics of Recombination 381-442 (Springer, 2007).
10. McKim, K. S. et al. Meiotic synapsis in the absence of recombination. Science 279, 876-878 (1998).
11. Dernburg, A. F. et al. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94, 387-398 (1998).
12. Phillips, C. M. et al. Identification of chromosome sequence motifs that mediate meiotic pairing and synapsis in C. elegans. Nat. Cell. Biol. 11, 934-942 (2009).
13. Lake, C. M., & Hawley, R. S. The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu. Rev. Physiol. 74, 425-451 (2012).
14. Hughes, S. E. et al. Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet. 5, e1000348 (2009).
15. Tsai, J. H., Yan, R., & McKee, B. D. Homolog pairing and sister chromatid cohesion in heterochromatin in Drosophila male meiosis I. Chromosoma 120, 335-351 (2011).
16. Tsai, J. H., & McKee, B. D. Homologous pairing and the role of pairing centers in meiosis. J. Cell Sci. 124, 1955-1963 (2011).
17. Hauf, S., & Watanabe, Y. Kinetochore orientation in mitosis and meiosis. Cell 119, 317-327 (2004).
18. Shao, T. et al. OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol. 156, 1386-1396 (2011).
19. Wang, M. et al. OsSGO1 maintains synaptonemal complex stabilization in addition to protecting centromeric cohesion during rice meiosis. Plant J. 67, 583-594 (2011).
20. Monje-Casas, F., Prabhu, V. R., Lee, B. H., Boselli, M., & Amon, A. Kinetochore orientation during meiosis is controlled by Aurora B and the monopolin complex. Cell 128, 477-490 (2007).
21. Li, X. X., & Dawe, R. K. Fused sister kinetochores initiate the reductional division in meiosis I. Nat. Cell Biol. 11, 1103-U1122 (2009).
22. Ishiguro, T., Tanaka, K., Sakuno, T., & Watanabe, Y. Shugoshin-PP2A counteracts casein-kinase-1-dependent cleavage of Rec8 by separase. Nat. Cell Biol. 12, 500-506 (2010).
23. Mola, L. M., & Papeschi, A. G. Holokinetic chromosomes at a glance. J. Basic Appl. Genet. 16, 1-4 (2006).
24. Guerra, M. et al. Neocentrics and holokinetics (holocentrics): chromosomes out of the centromeric rules. Cytogenet. Genome Res. 129, 82-96 (2010).
25. Melters, D. P., Paliulis, L. V., Korf, I. F., & Chan, S. W. Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res. 20, 579-593 (2012).
26. Dernburg, A. F. Here, there, and everywhere: kinetochore function on holocentric chromosomes. J. Cell Biol. 153, F33-F38 (2001).
27. Schvarzstein, M., Wignall, S. M., & Villeneuve, A. M. Coordinating cohesion, co-orientation, and congression during meiosis: lessons from holocentric chromosomes. Genes Dev. 24, 219-228 (2010).
28. Martinez-Perez, E. et al. Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. Genes Dev. 22, 2886-2901 (2008).
29. Wignall, S. M., & Villeneuve, A. M. Lateral microtubule bundles promote chromosome alignment during acentrosomal oocyte meiosis. Nat. Cell Biol. 11, 839-U135 (2009).
30. Dumont, J., Oegema, K., & Desai, A. A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis. Nat. Cell Biol. 12, 894-901 (2010).
31. Albertson, D. G., & Thomson, J. N. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1, 15-26 (1993).
32. Malheiros, N., Castro, D., & Cəmara, A. Cromosomas sem centrómero localizado. O caso de Luzula purpurea Link. Agron. Lusit. 9, 51-73 (1947).
33. Chandra, H. S. Inverse meiosis in triploid females of mealy bug, Planococcus citri. Genetics 47, 1441-1454 (1962).
34. Nordenskiold, H. Tetrad analysis and course of meiosis in three hybrids of Luzula campestris. Hereditas 47, 203-237 (1961).
35. Pazy, B., & Plitmann, U. Persisting demibivalents-A unique meiotic behavior in Cuscuta-babylonica choisy. Genome 29, 63-66 (1987).
36. Guerra, M., & Garcia, M. A. Heterochromatin and rDNA sites distribution in the holocentric chromosomes of Cuscuta approximata Bab. (Convolvulaceae). Genome 47, 134-140 (2004).
37. Da Silva, C. R. M., Gonzalez-Elizondo, M. S., & Vanzela, A. L. L. Reduction of chromosome number in Eleocharis subarticulata (Cyperaceae) by multiple translocations. Bot. J. Linn. Soc. 149, 457-464 (2005).
38. Bongiorni, S., Fiorenzo, P., Pippoletti, D., & Prantera, G. Inverted meiosis and meiotic drive in mealybugs. Chromosoma 112, 331-341 (2004).
39. Kusanagi, A. Mechanism of post-reductional meiosis in Luzula. Jpn. J. Genet. 37, 396-39 (1962).
40. Caryl, A. P., Armstrong, S. J., Jones, G. H., & Franklin, F. C. A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109, 62-71 (2000).
41. Armstrong, S. J., Caryl, A. P., Jones, G. H., & Franklin, F. C. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-Associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645-3655 (2002).
42. Li, W. et al. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc. Natl Acad. Sci. USA 101, 10596-10601 (2004).
43. Vanzela, A. L. L., Cuadrado, A., Jouve, N., Luceno, M., & Guerra, M. Multiple locations of the rDNA sites in holocentric chromosomes of Rhynchospora (Cyperaceae). Chromosome Res. 6, 345-349 (1998).
44. Vanzela, A. L. L., & Guerra, M. Heterochromatin differentiation in holocentric chromosomes of Rhynchospora (Cyperaceae). Genet. Mol. Biol. 23, 453-456 (2000).
45. Guerra, M. Patterns of heterochromatin distribution in plant chromosomes. Genet. Mol. Biol. 23, 1029-1041 (2000).
46. Sousa, A. et al. Distribution of 5S and 45S rDNA sites in plants with holokinetic chromosomes and the "chromosome field" hypothesis. Micron 42, 625-631 (2011).
47. Fujiwara, H., Nakazato, Y., Okazaki, S., & Ninaki, O. Stability and telomere structure of chromosomal fragments in two different mosaic strains of the silkworm, Bombyx mori. Zool. Sci. 17, 743-750 (2000).
48. San Martin, J. A. B., Andrade, C. G. T. D., Mastroberti, A. A., Mariath, J. E. D., & Vanzela, A. L. L. Asymmetric cytokinesis guide the development of pseudomonads in Rhynchospora pubera (Cyperaceae). Cell Biol. Int. 37, 203-212 (2013).
49. Vanzela, A. L. L., Cuadrado, A., & Guerra, M. Localization of 45S rDNA and telomeric sites on holocentric chromosomes of Rhynchospora tenuis Link (Cyperaceae). Genet. Mol. Biol. 26, 199-201 (2003).
50. Castiglione, M. R., & Cremonini, R. A fascinating island: 2n14 4. Plant Biosyst. 146, 711-726 (2012).
51. Pradillo, M. et al. An analysis of univalent segregation in meiotic mutants of Arabidopsis thaliana: a possible role for synaptonemal complex. Genetics 175, 505-511 (2007).
52. Pazy, B. Supernumerary chromosomes and their behaviour in meiosis of the holocentric Cuscuta babylonica Choisy. Bot. J. Linn. Soc. 123, 173-176 (1997).
53. Viera, A., Page, J., & Rufas, J. in Meiosis Vol. 5, 137-156 (Karger, 2009).
54. Papeschi, A. G., & Mola, L. M. Meiotic studies in Acanonicus-Hahni (Stal) (Coreidae, Heteroptera).1. Behavior of univalents in desynaptic individuals. Genetica 80, 31-38 (1990).
55. Heckmann, S. et al. Alternative meiotic chromatid segregation in the holocentric plant Luzulaelegans. Nat. Commun. 5, 4979 (2014).
56. Pedrosa, A., Sandal, N., Stougaard, J., Schweizer, D., & Bachmair, A. Chromosomal map of the model legume Lotus japonicus. Genetics 161, 1661-1672 (2002).
57. Wanzenbock, E. M., Schofer, C., Schweizer, D., & Bachmair, A. Ribosomal transcription units integrated via T-DNA transformation associate with the nucleolus and do not require upstream repeat sequences for activity in Arabidopsis thaliana. Plant J. 11, 1007-1016 (1997).
58. Demidov, D. et al. Anti-phosphorylated histone H2AThr120: a universal microscopic marker for centromeric chromatin of mono-And holocentric plant species. Cytogenet. Genome Res. 143, 150-156 (2014).
59. Manzanero, S., Arana, P., Puertas, M. J., & Houben, A. The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109, 308-317 (2000).
60. Chelysheva, L. et al. An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129, 143-153 (2010).
61. Peirson, B. N., Bowling, S. E., & Makaroff, C. A. A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant. Plant J. 11, 659-669 (1997).
62. Nagaki, K. et al. Sequencing of a rice centromere uncovers active genes. Nat. Genet. 36, 138-145 (2004).