Abstract
With respect to history, plants have provided an ideal system for cytogenetical analysis of the synaptonemal complex (SC). However, until recently, the identification of the genes that encode the SC in plants has proved elusive. In recent years, Arabidopsis thaliana was developed as a model system for plant meiosis research. As a result, there was substantial progress in the isolation of meiotic genes and this has recently led to the isolation of the first plant SC gene, ZYP1. The ZYP1 gene encodes a transverse filament (TF) protein that is predicted to have structural similarity to TF proteins found in other organisms. Analysis of plants deficient in ZYP1 expression has provided important insights into the function of the SC in plants. Loss of ZYP1 has only a limited effect on the overall level of recombination. However, it is associated with extensive nonhomologous recombination leading to multivalent formation at metaphase I. This phenomenon was not previously reported in other organisms. It is important to note that cytological analysis of the ZYP1 deficient lines indicates that SC formation is not required for the imposition of crossover interference.
Similar content being viewed by others
References
Albini SM (1994) A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis. Plant J 5:665–672
Alonso JM, Stepanova AN, Leisse TJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657
Anderson LK, Stack SM, Todd RJ, Ellis RP (1994) A monoclonal antibody to lateral element proteins in synaptonemal complexes of Lilium longiflorum. Chromosoma 103:357–367
Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Armstrong SJ, Jones GH (2003) Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. J Exp Bot 54:1–10
Armstrong SJ, Franklin FCH, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217
Beadle GW (1930) Genetic and cytological studies of a Mendelian asynaptic in Zea mays. Cornell Agric Exp Sta Mem 129:175–189
Beadle GW (1933) Further studies of asynaptic maize. Cytologia 4:269–287
Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris 316:1194–1199
Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear-complexes prior to meiotic chromosome synapsis. Cell 79:1081–1092
Bishop DK, Park D, Xu LZ, Kleckner N (1992) Dmc1 a meiosis-specific yeast homolog of Escherichia coli recA required for recombination, synaptonemal complex formation and cell-cycle progression. Cell 69:439–456
Bogdanov YF, Dadashev SY, Grishaeva TM (2003) In silico search for functionally similar proteins involved in meiosis and recombination in evolutionarily distant organisms. In Silico Biol 3:173–185
Borner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:9–15
Chen C, Zhang W, Timofejeva L, Gerardin Y, Ma H (2005) The Arabidopsis ROCK-N-ROLLERS gene encodes a homolog of the yeast ATP-dependent DNA helicase MER3 and is required for normal meiotic crossover formation. Plant J 43:321–334
de Vries FA, de Boer E, van den Bosch M, Baarends WM, Ooms M, Yuan L, Liu JG, van Zeeland AA, Heyting C, Pastink A (2005) Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev 19:1376–89
Doutriaux MP, Couteau F, Bergounioux C, White C (1998) Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol Gen Genet 257:283–291
Fawcett DW (1956) The fine structure of chromosomes in the meiotic prophase of vertebrate spermatocytes. J Cell Biol 2:403–406
Feldmann KA, Marks MD (1987) Agrobacterium mediated transformation of germinating seeds of Arabidopsis thaliana: a non-tissue culture approach. Mol Gen Genet 208:1–9
Fransz P, Armstrong S, Alonso-blanco C, Fischer TC, Torres-ruiz RA, Jones G (1998) Cytogenetics for the model system Arabidopsis thaliana. Plant J 13:867–876
Fung JC, Rockmill B, Odell M, Roeder GS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:795–802
Gillies CB (1975) Synaptonemal complex and chromosome structure. Annu Rev Genet 9:91–109
Golubovskaya IN, Mashnenkov AS (1976) Genetic control of meiosis: II. A desynaptic mutant in maize induced by N-nitroso-N-methyl-urea. Genetika 12:7–14
Golubovskaya IN, Grebennikova ZK, Auger DL, Sheridan WF (1997) The maize desynaptic1 mutation disrupts meiotic chromosome synapsis. Dev Genet 21:146–159
Golubovskaya IN, Harper LC, Pawlowski WP, Schichnes D, Cande WZ (2002) The pam1 gene is required for meiotic bouquet formation and efficient homologous synapsis in maize (Zea mays L.). Genetics 162:1979–1993
Havekes FW, de Jong JH, Heyting C, Ramanna MS (1994) Synapsis and chiasma formation in four meiotic mutants of tomato (Lycopersicon esculentum). Chromosome Res 2:315–325
Heyting C (1996) Synaptonemal complexes: structure and function. Curr Opin Cell Biol 8:389–396
Heyting C, Moens PB, van Raamsdonk W, Dietrich AJ, Vink AC, Redeker EJ (1987) Identification of two major components of the lateral elements of synaptonemal complexes of the rat. Eur J Cell Biol 43:148–154
Heyting C, Dietrich AJ, Moens PB, Dettmers RJ, Offenberg HH, Redeker EJ, Vink AC (1989) Synaptonemal complex proteins. Genome 31:81–87
Higgins JD, Armstrong SJ, Franklin FCH, Jones GH (2004) The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev 18:2557–2570
Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19:2488–2500
Hunt PA, Hassold TJ (2002) Sex matters in meiosis. Science 296:2181–2183
Jenkins G, Okumus A (1992) Indiscriminate synapsis in achiasmate Allium fistulosum L. (Liliaceae). J Cell Sci 103:415–422
Jones GH (1984) The control of chiasma distribution. SEB Symp 38:293–320
Klimyuk VI, Jones JDG (1997) AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J 11:1–14
Lammers JH, Offenberg HH, van Aalderen M, Vink AC, Dietrich AJ, Heyting C (1994) The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 14:1137–1146
Loidl J (1994) Cytological aspects of meiotic recombination. Experientia 50:285–294
MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM (2002) Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev 16:2428–2442
Maguire MP, Paredes AM, Riess RW (1991) The desynaptic mutant of maize as a combined defect of synaptonemal complex and chiasma maintenance. Genome 34:879–887
Martinez M, Naranjo T, Cuadrado C, Romero C (2001a) The synaptic behaviour of Triticum turgidum with variable doses of the PH1 locus. Theor Appl Genet 102:751–758
Martinez M, Cuñado N, Carcelén N, Romero C (2001b) The Ph1 and Ph2 loci play different roles in the synaptic behaviour of hexaploid wheat. Theor Appl Genet 103:398–405
Martinez M, Cuadrado C, Laurie DA, Romero C (2005) Synaptic behaviour of hexaploid wheat haploids with different effectiveness of the diploidizing mechanism. Cytogenet Genome Res 109:210–214
Martinez-Perez E, Shaw P, Aragon-Alcaide L, Moore G (2003) Chromosomes form into seven groups in hexaploid and tetraploid wheat as a prelude to meiosis. Plant J 36:21–29
Mello-Sampayo T, Canas AP (1973) Suppressors of meiotic chromosome pairing in common wheat. Proceedings of the 4th international wheat genetics symposium, pp 709–713
Mercier R, Jolivet S, Vezon D, Huppe E, Chelysheva L, Giovanni M, Nogué F, Doutriaux M, Horlow C, Grelon G (2005) Two meiotic crossover classes cohabit in Arabidopsis: one is dependent on MER3, whereas the other one is not. Curr Biol 15:692–701
Meuwissen RLJ, Offenberg HH, Dietrich AJJ, Riesewijk A, van Iersel M, Heyting C (1992) A coiled-coil related protein specific for synapsed regions of meiotic prophase chromosomes. EMBO J 11:5091–5100
Meuwissen RLJ, Meerts I, Hoovers JMN, Leschot NJ, Heyting C (1997) Human synaptonemal complex protein 1 (SCP1): isolation and characterization of the cDNA and chromosomal localization of the gene. Genomics 39:377–384
Moens P, Heyting C, Dietrich A, van Raamsdonk W, Chen Q (1987) Synaptonemal complex antigen location and conservation. J Cell Biol 105:93–103
Moses MJ (1956) Chromosomal structures in crayfish spermatocytes. J Cell Biol 2:215–218
Motamayor JC, Vezon D, Bajon C, Sauvanet A, Grandjean O, Marchand M, Bechtold N, Pelletier G, Horlow C (2000) Switch (swi1), an Arabidopsis thaliana mutant affected in the female meiotic switch. Sex Plant Reprod 12:209–218
Nelson OE, Clary GB (1952) Genetic control of semisterility in maize. J Hered 43:205–210
Offenberg HH, Dietrich AJ, Heyting C (1991) Tissue distribution of two major components of synaptonemal complexes of the rat. Chromosoma 101:83–91
Offenberg H, Schalk J, Meuwissen R, van Aalderen M, Kester H, Dietrich A, Heyting C (1998) SCP2: a major protein component of the axial elements of synaptonemal complexes of the rat. Nucleic Acids Res 26:2572–2579
Ohyama T, Iwaikawa Y, Toshiyuki K, Hotta Y, Tabata S (1992) Isolation of synaptonemal complexes from lily microsporocytes. Plant Sci 86:115–124
Ostergaard L, Yanofsky MF (2004) Establishing gene function by mutagenesis in Arabidopsis thaliana. Plant J 39:682–696
Page SL, Hawley RS (2001) c(3)G encodes a Drosophila synaptonemal complex protein. Genes Dev 15:3130–3143
Pawlowski WP, Golubovskaya IN, Timofejeva L, Meeley RB, Sheridan WF, Cande WZ (2004) Coordination of meiotic recombination, pairing, and synapsis by PHS1. Science 303:89–92
Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715
Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4:507–516
Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B, Franklin FCH, Jones GH (1997) Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res 5:551–559
Sanchez-Moran E, Mercier R, Higgins JD, Armstrong SJ, Jones GH, Franklin FCH (2005) A strategy to investigate the plant meiotic proteome. Cytogenet Genome Res 109:181–189
Sears ER, Okamoto M (1958) Intergenomic chromosome relationships in hexaploid wheat. Proc Tenth Int Cong Genet 2:258–259
Smith A, Benavente R (1992) Identification of a structural protein component of rat synaptonemal complexes. Exp Cell Res 198:291–297
Sosnikhina SP, Mikhailova EI, Tikholiz OA, Priyatkina SN, Smirnov VG, Dadashev SY, Kolomiets OL, Bogdanov YF (2005) Meiotic mutations in rye Secale cereale L. Cytogenet Genome Res 109:215–220
Storlazzi A, Xu L, Schwacha A, Kleckner N (1996) Synaptonemal complex (SC) component Zip1 plays a role in meiotic recombination independent of SC polymerization along the chromosomes. Philipp Numis Monogr 93:9043–9048
Suzuki M (1989) SPXX, a frequent sequence motif in gene regulatory proteins. J Mol Biol 207:61–84
Sym M, Roeder GS (1994) Crossover interference is abolished in the absence of a synaptonemal complex protein. Cell 79:283–292
Sym M, Engebrecht JA, Roeder GS (1993) ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis. Cell 72:365–378
Timopheeva LP, Golubovskaya IN (1991) A new type of desynaptic gene in maize revealed by the micro-spreading method of synaptonemal complexes. Cytologia 33:3–8
Tsubouchi T, Roeder GS (2005) A synaptonemal complex protein promotes homology-independent centromere coupling. Science 308:870–873
von Wettstein D, Rasmussen SW, Holm PB (1984) The synaptonemal complex in genetic segregation. Annu Rev Genet 18:331–411
Westergaard M, von Wettstein D (1972) The synaptonemal complex. Annu Rev Genet 6:71–110
Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754
Acknowledgements
We would like to thank Dr. Juan Luis Santos and Dr. Nieves Cuñado (Facultad de CC Biologicas, Universidad Complutense de Madrid, Spain) for kindly communicating their unpublished observations of the localization of ZYP1 in diploid wheat and providing the image used in Fig. 2. Work in the FCHF/GHJ laboratory is funded by the Biotechnology and Biological Sciences Research Council, UK.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by R. Benavente
The synaptonemal complex—50 years
Rights and permissions
About this article
Cite this article
Osman, K., Sanchez-Moran, E., Higgins, J.D. et al. Chromosome synapsis in Arabidopsis: analysis of the transverse filament protein ZYP1 reveals novel functions for the synaptonemal complex. Chromosoma 115, 212–219 (2006). https://doi.org/10.1007/s00412-005-0042-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-005-0042-4