The maize (Zea mays) desynaptic (dy) mutation defines a pathway for meiotic chromosome segregation, linking nuclear morphology, telomere distribution and synapsis

Journal of Cell Science

Volumn 125, Issue 15, 2012, Pages 3681-3690

  Murphy, Shaun P ^a   Bass, Hank W ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Maize; Meiosis; Nuclear envelope; SUN3; Telomeres

Indexed keywords

MESSENGER RNA; PLANT DNA;

ANAPHASE; ARTICLE; CELL NUCLEUS MEMBRANE; CELL STRUCTURE; CHROMOSOME 3; CHROMOSOME MAP; CHROMOSOME PAIRING; CHROMOSOME SEGREGATION; FOLLOW UP; GAIN OF FUNCTION MUTATION; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC LINKAGE; HEMIZYGOSITY; MAIZE; MEIOSIS; MUTATION; PACHYTENE; PHENOTYPE; PLANT GENETICS; POLLEN; PRIORITY JOURNAL; PROPHASE; PROTEIN DOMAIN; TELOMERE;

CELL NUCLEUS; CHROMOSOME SEGREGATION; GENETIC LINKAGE; IN SITU HYBRIDIZATION, FLUORESCENCE; MEIOSIS; MUTATION; SYNAPSES; TELOMERE; ZEA MAYS;

FUNGI/METAZOA GROUP; SYNAPSIS; ZEA MAYS;

EID: 84869140954     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.108290     Document Type: Article

References (53)

1. Abramoff, M. D., Magalhaes, P. J. and Ram, S. J. (2004). Image processing with ImageJ. Biophotonics Int. 11, 36-42.
2. Armstrong, S. J., Caryl, A. P., Jones, G. H. and Franklin, F. C. (2002). Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. 115, 3645-3655.
3. Bass, H. W. (2003). Telomere dynamics unique to meiotic prophase: formation and significance of the bouquet. Cell. Mol. Life Sci. 60, 2319-2324.
4. Bass, H. W., Marshall, W. F., Sedat, J. W., Agard, D. A. and Cande, W. Z. (1997). Telomeres cluster de novo before the initiation of synapsis: a three-dimensional spatial analysis of telomere positions before and during meiotic prophase. J. Cell Biol. 137, 5-18.
5. Bass, H. W., Bordoli, S. J. and Foss, E. M. (2003). The desynaptic (dy) and desynaptic1 (dsy1) mutations in maize (Zea mays L) cause distinct telomere- misplacement phenotypes during meiotic prophase. J. Exp. Bot. 54, 39-46.
6. Beckett, J. B. (1978). B-A translocations in maize. 1. Use in locating genes by chromosome arms. J. Hered. 69, 27-36.
7. Bennett, M. D., Lewis, K. R. and Harberd, D. J. (1977). The time and duration of meiosis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 277, 201-226.
8. Cande, W. Z., Golubovskaya, I., Wang, R. and Harper, L. (2009). Meiotic genes and meiosis in maize. In The Maize Handbook II: Genetics and Genomics (ed. J. L. Bennetzen and S. Hake), pp. 353-373. New York: Springer.
9. Caryl, A. P., Armstrong, S. J., Jones, G. H. and Franklin, F. C. (2000). A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1. Chromosoma 109, 62-71.
10. Chang, M. T. and Neuffer, M. G. (1989). Maize microsporogenesis. Genome 32, 232- 244.
11. Chikashige, Y. and Hiraoka, Y. (2001). Telomere binding of the Rap1 protein is required for meiosis in fission yeast. Curr. Biol. 11, 1618-1623.
12. Conrad, M. N., Lee, C. Y., Wilkerson, J. L. and Dresser, M. E. (2007). MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104, 8863-8868.
13. Cooper, J. P., Watanabe, Y. and Nurse, P. (1998). Fission yeast Taz1 protein is required for meiotic telomere clustering and recombination. Nature 392, 828-831.
14. Davis, G. L., McMullen, M. D., Baysdorfer, C., Musket, T., Grant, D., Staebell, M., Xu, G., Polacco, M., Koster, L., Melia-Hancock, S. et al. (1999). A maize map standard with sequenced core markers, grass genome reference points and 932 expressed sequence tagged sites (ESTs) in a 1736-locus map. Genetics 152, 1137- 1172.
15. Dellaporta, S. L., Wood, J. and Hicks, J. B. (1985). Maize DNA miniprep. Plant Mol. Biol. Rep. 30, 36-38.
16. Ding, X., Xu, R., Yu, J., Xu, T., Zhuang, Y. and Han, M. (2007). SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12, 863-872.
17. Dole, J. and Weber, D. F. (2007). Detection of quantitative trait Loci influencing recombination using recombinant inbred lines. Genetics 177, 2309-2319.
18. Esch, E., Szymaniak, J. M., Yates, H., Pawlowski, W. P. and Buckler, E. S. (2007). Using crossover breakpoints in recombinant inbred lines to identify quantitative trait loci controlling the global recombination frequency. Genetics 177, 1851-1858.
19. Franklin, A. E., Golubovskaya, I. N., Bass, H. W. and Cande, W. Z. (2003). Improper chromosome synapsis is associated with elongated RAD51 structures in the maize desynaptic2 mutant. Chromosoma 112, 17-25.
20. Golubovskaya, I. N. and Mashnenkov, A. S. (1977). Multiple disturbances of meiosis in corn caused by a single recessive mutation pamA-A344. Genetica 13, 1910-1931
21. Golubovskaya, I. N., Harper, L. C., Pawlowski, W. P., Schichnes, D. and Cande, W. Z. (2002). The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162, 1979-1993.
22. Golubovskaya, I., Sheridan, W., Harper, L. and Cande, W. Z. (2003). New meiotic mutants of maize identified from Mu transposon and EMS mutant screens. Maize Genet. Coop. Newsl. 77, 10-13.
23. Golubovskaya, I. N., Hamant, O., Timofejeva, L., Wang, C. J., Braun, D., Meeley, R. and Cande, W. Z. (2006). Alleles of afd1 dissect REC8 functions during meiotic prophase I. J. Cell Sci. 119, 3306-3315.
24. Golubovskaya, I. N., Wang, C. J., Timofejeva, L. and Cande, W. Z. (2011). Maize meiotic mutants with improper or non-homologous synapsis due to problems in pairing or synaptonemal complex formation. J. Exp. Bot. 62, 1533-1544.
25. Graumann, K., Runions, J. and Evans, D. E. (2010). Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 61, 134-144.
26. Harper, L., Golubovskaya, I. and Cande, W. Z. (2004). A bouquet of chromosomes. J. Cell Sci. 117, 4025-4032.
27. Hiraoka, Y. and Dernburg, A. F. (2009). The SUN rises on meiotic chromosome dynamics. Dev. Cell 17, 598-605.
28. Ji, Y., Stelly, D. M., De Donato, M., Goodman, M. M. and Williams, C. G. (1999). A candidate recombination modifier gene for Zea mays L. Genetics 151, 821-830.
29. John, B. (ed.) (1990). Meiosis (Developmental and Cell Biology Series 22). New York; Cambridge University Press.
30. Lawrence, C. J., Seigfried, T. E., Bass, H. W. and Anderson, L. K. (2006). Predicting chromosomal locations of genetically mapped loci in maize using the Morgan2McClintock Translator. Genetics 172, 2007-2009.
31. Maguire, M. P. and Jackson, J. D. (1998). Two well-known mutants of chiasma maintenance function in maize are allelic. Genome 41, 417-421.
32. Maguire, M. P., Paredes, A. M. and Riess, R. W. (1991). The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance. Genome 34, 879-887.
33. Maguire, M. P., Riess, R. W. and Paredes, A. M. (1993). Evidence from a maize desynaptic mutant points to a probable role of synaptonemal complex central region components in provision for subsequent chiasma maintenance. Genome 36, 797-807
34. Michelmore, R. W., Paran, I. and Kesseli, R. V. (1991). Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl. Acad. Sci. USA 88, 9828-9832.
35. Mikhailova, E. I., Phillips, D., Sosnikhina, S. P., Lovtsyus, A. V., Jones, R. N. and Jenkins, G. (2006). Molecular assembly of meiotic proteins Asy1 and Zyp1 and pairing promiscuity in rye (Secale cereale L.) and its synaptic mutant sy10. Genetics 174, 1247-1258.
36. Moriguchi, K., Suzuki, T., Ito, Y., Yamazaki, Y., Niwa, Y. and Kurata, N. (2005). Functional isolation of novel nuclear proteins showing a variety of subnuclear localizations. Plant Cell 17, 389-403.
37. Murphy, S. P. and Bass, H. W. (2012). Genetics and cytology of meiotic chromosome behavior in plants. In Plant Genetics and Genomics: Crops and Models. Vol. 4 (ed. H. W. Bass and J. W. Brichler), pp. 193-229. New York: Springer.
38. Murphy, S. P., Simmons, C. R. and Bass, H. W. (2010). Structure and expression of the maize (Zea mays L.) SUN-domain protein gene family: evidence for the existence of two divergent classes of SUN proteins in plants. BMC Plant Biol. 10, 269.
39. Nelson, O. N. and Clary, G. B. (1952). Genic control of semi-sterility in maize. J. Hered. 43, 205-210.
40. Oda, Y. and Fukuda, H. (2011). Dynamics of Arabidopsis SUN proteins during mitosis and their involvement in nuclear shaping. Plant J. 66, 629-641.
41. Pawlowski, W. P., Wang, C. J., Golubovskaya, I. N., Szymaniak, J. M., Shi, L., Hamant, O., Zhu, T., Harper, L., Sheridan, W. F. and Cande, W. Z. (2009). Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proc. Natl. Acad. Sci. USA 106, 3603-3608.
42. Sanchez-Moran, E., Santos, J. L., Jones, G. H. and Franklin, F. C. (2007). ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Genes Dev. 21, 2220-2233.
43. Sanchez-Moran, E., Osman, K., Higgins, J. D., Pradillo, M., Cuñado, N., Jones, G. H. and Franklin, F. C. (2008). ASY1 coordinates early events in the plant meiotic recombination pathway. Cytogenet. Genome Res. 120, 302-312.
44. Scherthan, H. (2007). Telomere attachment and clustering during meiosis. Cell. Mol. Life Sci. 64, 117-124.
45. Scherthan, H. (2009). Analysis of telomere dynamics in mouse spermatogenesis. Methods Mol. Biol. 558, 383-399.
46. Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Härle, M. and Cremer, T. (1996). Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing. J. Cell Biol. 134, 1109- 1125.
47. Schmitt, J., Benavente, R., Hodzic, D., Höög, C., Stewart, C. L. and Alsheimer, M. (2007). Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope. Proc. Natl. Acad. Sci. USA 104, 7426-7431.
48. Starr, D. A. (2009). A nuclear-envelope bridge positions nuclei and moves chromosomes. J. Cell Sci. 122, 577-586.
49. Starr, D. A. and Fridolfsson, H. N. (2010). Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26, 421-444.
50. Trelles-Sticken, E., Dresser, M. E. and Scherthan, H. (2000). Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151, 95-106.
51. Van Damme, D., Bouget, F. Y., Van Poucke, K., Inzé, D. and Geelen, D. (2004). Molecular dissection of plant cytokinesis and phragmoplast structure: a survey of GFP-tagged proteins. Plant J. 40, 386-398.
52. Wang, C. J., Carlton, P. M., Golubovskaya, I. N. and Cande, W. Z. (2009). Interlock formation and coiling of meiotic chromosome axes during synapsis. Genetics 183, 905-915.
53. Zhou, X., Graumann, K., Evans, D. E. and Meier, I. (2012). Novel plant SUN-KASH bridges are involved in RanGAP anchoring and nuclear shape determination. J. Cell Biol. 196, 203-211.