The novel gene Homologous Pairing Aberration In Rice Meiosis1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis

Plant Cell

Volumn 16, Issue 4, 2004, Pages 1008-1020

  Nonomura, Ken Ichi ^a   Nakano, Mutsuko ^a   Fukuda, Toshiyuki ^a,b   Eiguchi, Mitsugu ^a   Miyao, Akio ^c   Hirochika, Hirohiko ^c   Kurata, Nori ^a,b  

^a NATIONAL INSTITUTE OF GENETICS   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CHROMOSOMES; CYTOLOGY; GENETIC ENGINEERING; PROTEINS; STERILIZATION (CLEANING);

ANAPHASE; CYTOKINESIS; GAMETES; TELOPHASE;

PLANT CELL CULTURE;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; EUKARYOTA; ORYZA SATIVA;

EID: 1842712462     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.020701     Document Type: Article

References (75)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
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. Armstrong, S.J., Franklin, F.C., and Jones, G.H. (2001). Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. 114, 4207-4217.
4. Bai, X., Peirson, B.N., Dong, F., Xue, C., and Makaroff, C.A. (1999). Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 11, 417-430.
5. 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.
6. Bergerat, A., de Massy, B., Gadelle, D., Varoutas, P.C., Nicolas, A., and Forterre, P. (1997). An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386, 414-417.
7. Bhatt, A.M., Lister, C., Page, T., Fransz, P., Findlay, K., Jones, G.H., Dickinson, H.G., and Dean, C. (1999). The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. 19, 463-472.
8. Cal, X., Dong, F., Edelmann, R.E., and Makaroff, C.A. (2003). The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing. J. Cell Sci. 116, 2999-3007.
9. Cao, L., Alani, E., and Kleckner, N. (1990). A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell 61, 1089-1101.
10. 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.
11. Celerin, M., Merino, S.T., Stone, J.E., Menzie, A.M., and Zolan, M.E. (2000). Multiple roles of Spo11 in meiotic chromosome behavior. EMBO J. 19, 2739-2750.
12. Chan, A., and Cande, W.Z. (1998). Maize meiotic spindles assemble around chromatin and do not require paired chromosomes. J. Cell Sci. 111, 3507-3515.
13. Chelsky, D., Ralph, R., and Jonak, G. (1989). Sequence requirements for synthetic peptide-mediated translocation to the nucleus. Mol. Cell. Biol. 9, 2487-2492.
14. Chikashige, Y., Ding, D.Q., Funabiki, H., Haraguchi, T., Mashiko, S., Yanagida, M., and Hiraoka, Y. (1994). Telomere-led premeiotic chromosome movement in fission yeast. Science 264, 270-273.
15. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996). Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.
16. Chou, P.Y., and Fasman, G.D. (1978). Prediction of the secondary structure of proteins from their amino acid sequence. Adv. Enzymol. Relat. Areas Mol. Biol. 47, 45-148.
17. Combet, C., Blanchet, C., Geourjon, C., and Deleage, G. (2000). NPS@: Network protein sequence analysis. Trends Biochem. Sci. 25, 147-150.
18. 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.
19. Couteau, F., Belzile, F., Horlow, C., Grandjean, O., Vezon, D., and Doutriaux, M.P. (1999). Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11, 1623-1634.
20. Fassler, J., Landsman, D., Acharya, A., Moll, J.R., Bonovich, M., and Vinson, C. (2002). B-ZIP proteins encoded by the Drosophila genome: Evaluation of potential dimerization partners. Genome Res. 12, 1190-1200.
21. Fuse, T., Sasaki, T., and Yano, M. (2001). Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219-222.
22. Gillies, C.B. (1975). Synaptonemal complex and chromosome structure. Annu. Rev. Genet. 9, 91-109.
23. Giroux, C.N., Dresser, M.E., and Tiano, H.F. (1989). Genetic control of chromosome synapsis in yeast meiosis. Genome 31, 88-94.
24. Glover, J., Grelon, M., Craig, S., Chaudhury, A., and Dennis, E. (1998). Cloning and characterization of MS5 from Arabidopsis: A gene critical in male meiosis. Plant J. 15, 345-356.
25. 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.
26. Grelon, M., Gendrot, G., Vezon, D., and Pelletier, G. (2003). 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 J. 35, 465-475.
27. Grelon, M., Vezon, D., Gendrot, G., and Pelletier, G. (2001). AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J. 20, 589-600.
28. Hiei, Y., Ohta, S., Komari, T., and Kumashiro, T. (1994). Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282.
29. Hirano, T. (2000). Chromosome cohesion, condensation, and separation. Annu. Rev. Biochem. 69, 115-144.
30. Hiraoka, Y. (1998). Melotic telomeres: A matchmaker for homologous chromosomes. Genes Cells 3, 405-413.
31. Hirochika, H., Sugimoto, K., Otsuki, Y., Tsugawa, H., and Kanda, M. (1996). Retrotransposons of rice involved in mutations induced by tissue culture. Proc. Natl. Acad. Sci. USA 93, 7783-7788.
32. Hollingsworth, N.M., Goetsch, L., and Byers, B. (1990). The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell 61, 73-84.
33. Ikemoto, S., Nakamura, T., Kubo, M., and Shimoda, C. (2000). S. pombe sporulation-specific coiled-coil protein Spo15p is localized to the spindle pole body and essential for its modification. J. Cell Sci. 113, 545-554.
34. Kitada, K., Kurata, N., Satoh, H., and Omura, T. (1983). Genetic control of meiosis in rice, Oryza sativa L. I. Classification of meiotic mutants induced by MNU and their cytogenetical characteristics. Jpn. J. Genet. 58, 231-240.
35. Kitada, K., and Omura, T. (1983). Genetic control of meiosis in rice Oryza sativa L. II. Cytogenetical analyses of desynaptic mutants. Jpn. J. Genet. 58, 567-577.
36. Landschulz, W.H., Johnson, P.F., and McKnight, S.L. (1988). The leucine zipper: A hypothetical structure common to a new class of DNA binding proteins. Science 240, 1759-1764.
37. Leu, J.Y., Chua, P.R., and Roeder, G.S. (1998). The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell 94, 375-386.
38. Loidl, J. (1988). The effect of colchicine on synaptonemal complex formation in Allium ursinum. Exp. Cell Res. 178, 93-97.
39. Loidl, J., Klein, F., and Scherthan, H. (1994). Homologous pairing is reduced but not abolished in asynaptic mutants of yeast. J. Cell Biol. 125, 1191-1200.
40. Martinez-Perez, E., Shaw, P., Reader, S., Aragon-Alcaide, L., Miller, T., and Moore, G. (1999). Homologous chromosome pairing in wheat. J. Cell Sci. 112, 1761-1769.
41. Mercier, R., Armstrong, S.J., Horlow, C., Jackson, N.P., Makaroff, C.A., Vezon, D., Pelletier, G., Jones, G.H., and Franklin, F.C. (2003). The meiotic protein SWI1 is required for axial element formation and recombination initiation in Arabidopsis. Development 130, 3309-3318.
42. Mercier, R., Vezon, D., Bullier, E., Motamayor, J.C., Sellier, A., Lefevre, F., Pelletier, G., and Horlow, C. (2001). SWITCH1 (SWI1): A novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev. 15, 1859-1871.
43. Meuwissen, R.L., Offenberg, H.H., Dietrich, A.J., Riesewijk, A., vanlersel, M., and Heyting, C. (1992). A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J. 11, 5091-5100.
44. Moens, P.B. (1969). The fine structure of meiotic chromosome polarization and pairing in Locusta migratoria spermatocytes. Chromosoma 28, 1-25.
45. Moitra, J., Szilak, L., Krylov, D., and Vinson, C. (1997). Leucine is the most stabilizing aliphatic amino acid in the d position of a dimeric leucine zipper coiled coil. Biochemistry 36, 12567-12573.
46. Nabeshima, K., Kakihara, Y., Hiraoka, Y., and Nojima, H. (2001). A novel meiosis-specific protein of fission yeast, Meu13p, promotes homologous pairing independently of homologous recombination. EMBO J. 20, 3871-3881.
47. Nimmo, E.R., Pidoux, A.L., Perry, P.E., and Allshire, R.C. (1998). Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature 392, 825-828.
48. Niwa, O., Shimanuki, M., and Miki, F. (2000). Telomere-led bouquet formation facilitates homologous chromosome pairing and restricts ectopic interaction in fission yeast meiosis. EMBO J. 19, 3831-3840.
49. Nonomura, K.I., Miyoshi, K., Eiguchi, M., Suzuki, T., Miyao, A., Hirochika, H., and Kurata, N. (2003). The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728-1739.
50. Nonomura, K.I., Nakano, M., Murata, K., Miyoshi, K., Eiguchi, M., Miyao, A., Hirochika, H., and Kurata, N. (2004). The insertional mutation of rice PAIR2 gene, the ortholog of Arabidopsis ASY1, caused a defect in homologous chromosome pairing in meiosis. Mol. Genet. Genomics 271, 121-129.
51. Offenberg, H.H., Schalk, J.A., Meuwissen, R.L., van Aalderen, M., Kester, H.A., Dietrich, A.J., and Heyting, C. (1998). SCP2: A major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res. 26, 2572-2579.
52. Pawlowski, W.P., Golubovskaya, I.N., Timofejeva, L., Meeley, R.B., Sheridan, W.F., and Cande, W.Z. (2004). Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303, 89-92.
53. Peirson, B.N., Bowling, S.E., and Makaroff, C.A. (1997). A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant. Plant J. 11, 659-669.
54. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
55. Scherthan, H., Weich, S., Schwegler, H., Heyting, C., Harle, 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.
56. Schommer, C., Beven, A., Lawrenson, T., Shaw, P., and Sablowski, R. (2003). AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J. 36, 1-11.
57. Schwarzscher, T., and Heslop-Harrison, P. (2000). Practical in Situ Hybridization. (New York, NY: Springer-Verlag).
58. Shepard, J., Boothroyd, E.R., and Stern, H. (1974). The effect of colchicine on synapsis and chiasma formation in microsporocytes of Lilium. Chromosoma 44, 423-437.
59. Shimanuki, M., Miki, F., Ding, D.O., Chikashige, Y., Hiraoka, Y., Horio, T., and Niwa, O. (1997). A novel fission yeast gene, kms1 +, is required for the formation of meiotic prophase-specific nuclear architecture. Mol. Gen. Genet. 254, 238-249.
60. Sun, H., Treco, D., Schultes, N.P., and Szostak, J.W. (1989). Double-strand breaks at an initiation site for meiotic gene conversion. Nature 338, 87-90.
61. Suzuki, M. (1989). SPXX, a frequent sequence motif in gene regulatory proteins. J. Mol. Biol. 207, 61-84.
62. Takaiwa, F., Oono, K., Iida, Y., and Sugiura, M. (1985). The complete nucleotide sequence of a rice 25S rRNA gene. Gene 37, 255-259.
63. Thomas, J.B., and Kaltsikes, P.J. (1977). The effect of colchicine on chromosome pairing. Can. J. Gen. Cytol. 19, 231-249.
64. Tung, K.S., and Boeder, G.S. (1998). Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae. Genetics 149, 817-832.
65. Verma, D.P. (2001). Cytokinesis and building of the cell plate in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 751-784.
66. Vollbrecht, E., and Hake, S. (1995). Deficiency analysis of female gametogenesis in maize. Dev. Genet. 16, 44-63.
67. von Wettstein, D., Rasmussen, S.W., and Holm, P.B. (1984). The synaptonemal complex in genetic segregation. Annu. Rev. Genet. 18, 331-413.
68. Weiner, B.M., and Kleckner, N. (1994). Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77, 977-991.
69. Westergaard, M., and von Wettstein, D. (1972). The synaptonemal complex. Annu. Rev. Genet. 6, 71-110.
70. White, R.J., and Jackson, S.P. (1992). The TATA-binding protein: A central role in transcription by RNA polymerases I, II and III. Trends Genet. 8, 284-288.
71. Yamamoto, A., and Hiraoka, Y. (2001). How do meiotic chromosomes meet their homologous partners? Lessons from fission yeast. Bioessays 23, 526-533.
72. Yamashita, A., Watanabe, Y., and Yamamoto, M. (1997). Microtubule-associated coiled-coil protein Ssm4 is involved in the meiotic development in fission yeast. Genes Cells 2, 155-166.
73. Yamazaki, M., Tsugawa, H., Miyao, A., Yano, M., Wu, J., Yamamoto, S., Matsumoto, T., Sasaki, T., and Hirochika, H. (2001). The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol. Genet. Genomics 265, 336-344.
74. Yuan, L., Pelttari, J., Brundell, E., Bjorkroth, B., Zhao, J., Liu, J.G., Brismar, H., Daneholt, B., and Hoog, C. (1998). The synaptonemal complex protein SCP3 can form multistranded, cross-striated fibers in vivo. J. Cell Biol. 142, 331-339.
75. Zickler, D., and Kleckner, N. (1998). The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619-697.