Abstract
The proper pairing, recombination, and segregation of chromosomes are central to meiosis and sexual reproduction. The syn1 mutation was previously identified as a synaptic mutant in a T-DNA-tagged population of plants. SYN1 has been isolated and found to exhibit similarity to Schizosaccharomyces pombe RAD21 and RAD21-like proteins, which are required for chromosome condensation and sister chromatid cohesion during mitosis. Plants homozygous for syn1 are male and female sterile and show defects in chromosome condensation and pairing beginning at leptonema of meiosis I. Fragmentation of the chromosomes was observed at metaphase I. Alternative promoters produced two SYN1 transcripts. One transcript was expressed at low levels in most tissues, whereas the other was expressed only in prebolting buds. DNA blot analyses suggest that Arabidopsis contains a small RAD21 gene family. Consistent with the DNA blot data, a second Arabidopsis RAD21-like gene has been identified. These results suggest that different RAD21-like proteins play essential roles in chromosome condensation and pairing during both meiosis and mitosis.
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- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- An Y. Q., McDowell J. M., Huang S., McKinney E. C., Chambliss S., Meagher R. B. Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 1996 Jul;10(1):107–121. doi: 10.1046/j.1365-313x.1996.10010107.x. [DOI] [PubMed] [Google Scholar]
- Anderson L. K., Offenberg H. H., Verkuijlen W. M., Heyting C. RecA-like proteins are components of early meiotic nodules in lily. Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6868–6873. doi: 10.1073/pnas.94.13.6868. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beadle G. W. Genes in Maize for Pollen Sterility. Genetics. 1932 Jul;17(4):413–431. doi: 10.1093/genetics/17.4.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birkenbihl R. P., Subramani S. Cloning and characterization of rad21 an essential gene of Schizosaccharomyces pombe involved in DNA double-strand-break repair. Nucleic Acids Res. 1992 Dec 25;20(24):6605–6611. doi: 10.1093/nar/20.24.6605. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bishop D. K., Park D., Xu L., Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992 May 1;69(3):439–456. doi: 10.1016/0092-8674(92)90446-j. [DOI] [PubMed] [Google Scholar]
- Bishop D. K. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell. 1994 Dec 16;79(6):1081–1092. doi: 10.1016/0092-8674(94)90038-8. [DOI] [PubMed] [Google Scholar]
- Dawe R. Kelly. MEIOTIC CHROMOSOME ORGANIZATION AND SEGREGATION IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):371–395. doi: 10.1146/annurev.arplant.49.1.371. [DOI] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ftouhi-Paquin N., Hauer C. R., Stack R. F., Tarentino A. L., Plummer T. H., Jr Molecular cloning, primary structure, and properties of a new glycoamidase from the fungus Aspergillus tubigensis. J Biol Chem. 1997 Sep 5;272(36):22960–22965. doi: 10.1074/jbc.272.36.22960. [DOI] [PubMed] [Google Scholar]
- Glover J., Grelon M., Craig S., Chaudhury A., Dennis E. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J. 1998 Aug;15(3):345–356. doi: 10.1046/j.1365-313x.1998.00216.x. [DOI] [PubMed] [Google Scholar]
- Golubovskaya I., Grebennikova Z. K., Avalkina N. A., Sheridan W. F. The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics. 1993 Dec;135(4):1151–1166. doi: 10.1093/genetics/135.4.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Green I. R., Sargan D. R. Sequence of the cDNA encoding ovine tumor necrosis factor-alpha: problems with cloning by inverse PCR. Gene. 1991 Dec 30;109(2):203–210. doi: 10.1016/0378-1119(91)90610-n. [DOI] [PubMed] [Google Scholar]
- Guacci V., Koshland D., Strunnikov A. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell. 1997 Oct 3;91(1):47–57. doi: 10.1016/s0092-8674(01)80008-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hawley R. S., Arbel T. Yeast genetics and the fall of the classical view of meiosis. Cell. 1993 Feb 12;72(3):301–303. doi: 10.1016/0092-8674(93)90108-3. [DOI] [PubMed] [Google Scholar]
- Hebsgaard S. M., Korning P. G., Tolstrup N., Engelbrecht J., Rouzé P., Brunak S. Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 1996 Sep 1;24(17):3439–3452. doi: 10.1093/nar/24.17.3439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henderson S. A., Lu B. C. The use of haematoxylin for squash preparations of chromosomes. Stain Technol. 1968 Jul;43(4):233–236. doi: 10.3109/10520296809115074. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
- Heo S. J., Tatebayashi K., Kato J., Ikeda H. The RHC21 gene of budding yeast, a homologue of the fission yeast rad21+ gene, is essential for chromosome segregation. Mol Gen Genet. 1998 Jan;257(2):149–156. doi: 10.1007/s004380050634. [DOI] [PubMed] [Google Scholar]
- Higgins D. G., Sharp P. M. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. doi: 10.1093/bioinformatics/5.2.151. [DOI] [PubMed] [Google Scholar]
- Horton P., Nakai K. A probabilistic classification system for predicting the cellular localization sites of proteins. Proc Int Conf Intell Syst Mol Biol. 1996;4:109–115. [PubMed] [Google Scholar]
- Huang S. H. Inverse PCR. An efficient approach to cloning cDNA ends. Methods Mol Biol. 1997;67:287–294. doi: 10.1385/0-89603-483-6:287. [DOI] [PubMed] [Google Scholar]
- Jacobson A. Purification and fractionation of poly(A)+ RNA. Methods Enzymol. 1987;152:254–261. doi: 10.1016/0076-6879(87)52028-6. [DOI] [PubMed] [Google Scholar]
- Ji L. H., Langridge P. An early meiosis cDNA clone from wheat. Mol Gen Genet. 1994 Apr;243(1):17–23. doi: 10.1007/BF00283871. [DOI] [PubMed] [Google Scholar]
- Kleckner N. Meiosis: how could it work? Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8167–8174. doi: 10.1073/pnas.93.16.8167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klimyuk V. I., Jones J. D. AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J. 1997 Jan;11(1):1–14. doi: 10.1046/j.1365-313x.1997.11010001.x. [DOI] [PubMed] [Google Scholar]
- Kobayashi T., Kobayashi E., Sato S., Hotta Y., Miyajima N., Tanaka A., Tabata S. Characterization of cDNAs induced in meiotic prophase in lily microsporocytes. DNA Res. 1994;1(1):15–26. doi: 10.1093/dnares/1.1.15. [DOI] [PubMed] [Google Scholar]
- Lin Y., Larson K. L., Dorer R., Smith G. R. Meiotically induced rec7 and rec8 genes of Schizosaccharomyces pombe. Genetics. 1992 Sep;132(1):75–85. doi: 10.1093/genetics/132.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Losada A., Hirano M., Hirano T. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev. 1998 Jul 1;12(13):1986–1997. doi: 10.1101/gad.12.13.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maguire M. P., Riess R. W., Paredes A. M. Evidence from a maize desynaptic mutant points to a probable role of synaptonemal complex central region components in provision for subsequent chiasma maintenance. Genome. 1993 Oct;36(5):797–807. doi: 10.1139/g93-105. [DOI] [PubMed] [Google Scholar]
- McKay M. J., Troelstra C., van der Spek P., Kanaar R., Smit B., Hagemeijer A., Bootsma D., Hoeijmakers J. H. Sequence conservation of the rad21 Schizosaccharomyces pombe DNA double-strand break repair gene in human and mouse. Genomics. 1996 Sep 1;36(2):305–315. doi: 10.1006/geno.1996.0466. [DOI] [PubMed] [Google Scholar]
- Michaelis C., Ciosk R., Nasmyth K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell. 1997 Oct 3;91(1):35–45. doi: 10.1016/s0092-8674(01)80007-6. [DOI] [PubMed] [Google Scholar]
- Miyazaki W. Y., Orr-Weaver T. L. Sister-chromatid cohesion in mitosis and meiosis. Annu Rev Genet. 1994;28:167–187. doi: 10.1146/annurev.ge.28.120194.001123. [DOI] [PubMed] [Google Scholar]
- Molnar M., Bähler J., Sipiczki M., Kohli J. The rec8 gene of Schizosaccharomyces pombe is involved in linear element formation, chromosome pairing and sister-chromatid cohesion during meiosis. Genetics. 1995 Sep;141(1):61–73. doi: 10.1093/genetics/141.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ogawa T., Shinohara A., Nabetani A., Ikeya T., Yu X., Egelman E. H., Ogawa H. RecA-like recombination proteins in eukaryotes: functions and structures of RAD51 genes. Cold Spring Harb Symp Quant Biol. 1993;58:567–576. doi: 10.1101/sqb.1993.058.01.063. [DOI] [PubMed] [Google Scholar]
- Orr-Weaver T. L. Meiosis in Drosophila: seeing is believing. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10443–10449. doi: 10.1073/pnas.92.23.10443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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. 1997 Apr;11(4):659–669. doi: 10.1046/j.1365-313x.1997.11040659.x. [DOI] [PubMed] [Google Scholar]
- Rechsteiner M., Rogers S. W. PEST sequences and regulation by proteolysis. Trends Biochem Sci. 1996 Jul;21(7):267–271. [PubMed] [Google Scholar]
- Roeder G. S. Sex and the single cell: meiosis in yeast. Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10450–10456. doi: 10.1073/pnas.92.23.10450. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ross K. J., Fransz P., Armstrong S. J., Vizir I., Mulligan B., Franklin F. C., Jones G. H. Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res. 1997 Dec;5(8):551–559. doi: 10.1023/a:1018497804129. [DOI] [PubMed] [Google Scholar]
- Ross K. J., Fransz P., Jones G. H. A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. 1996 Nov;4(7):507–516. doi: 10.1007/BF02261778. [DOI] [PubMed] [Google Scholar]
- Sato S., Hotta Y., Tabata S. Structural analysis of a recA-like gene in the genome of Arabidopsis thaliana. DNA Res. 1995;2(2):89–93. doi: 10.1093/dnares/2.2.89. [DOI] [PubMed] [Google Scholar]
- Sieburth L. E., Meyerowitz E. M. Molecular dissection of the AGAMOUS control region shows that cis elements for spatial regulation are located intragenically. Plant Cell. 1997 Mar;9(3):355–365. doi: 10.1105/tpc.9.3.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spielman M., Preuss D., Li F. L., Browne W. E., Scott R. J., Dickinson H. G. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development. 1997 Jul;124(13):2645–2657. doi: 10.1242/dev.124.13.2645. [DOI] [PubMed] [Google Scholar]
- Terasawa M., Shinohara A., Hotta Y., Ogawa H., Ogawa T. Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev. 1995 Apr 15;9(8):925–934. doi: 10.1101/gad.9.8.925. [DOI] [PubMed] [Google Scholar]
- Verwoerd T. C., Dekker B. M., Hoekema A. A small-scale procedure for the rapid isolation of plant RNAs. Nucleic Acids Res. 1989 Mar 25;17(6):2362–2362. doi: 10.1093/nar/17.6.2362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu S., Ozawa M., Naved A. F., Miyauchi T., Muramatsu H., Muramatsu T. cDNA cloning and sequence analysis of a novel calcium binding protein with oligoproline motif. Cell Struct Funct. 1995 Aug;20(4):263–268. doi: 10.1247/csf.20.263. [DOI] [PubMed] [Google Scholar]
- Zetka M., Rose A. The genetics of meiosis in Caenorhabditis elegans. Trends Genet. 1995 Jan;11(1):27–31. doi: 10.1016/s0168-9525(00)88983-0. [DOI] [PubMed] [Google Scholar]