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Improper Chromosome Synapsis Is Associated with Elongated RAD51 Structures in the Maize Desynaptic2 Mutant

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Improper Chromosome Synapsis Is Associated with Elongated RAD51 Structures in the Maize Desynaptic2 Mutant Chromosoma (2003) 112:17–25 DOI 10.1007/s00412-003-0242-8 ORIGINAL ARTICLE Amie E. Franklin · Inna N. Golubovskaya · Hank W. Bass · W. Zacheus Cande Improper chromosome synapsis is associated with elongated RAD51 structures in the maize desynaptic2 mutant Received: 27 November 2002 / Revised: 17 March 2003 / Accepted: 24 April 2003 / Published online: 14 June 2003 Springer-Verlag 2003 Abstract The RecA homolog, RAD51, performs a cen- served throughout the eukaryotic superkingdom (John tral role in catalyzing the DNA strand exchange event of 1990). During meiotic prophase, chromosomes identify meiotic recombination. During meiosis, RAD51 com- their homologous partners and undergo homologous plexes develop on pairing chromosomes and then most recombination. In many organisms, homologous chromo- disappear upon synapsis. In the maize meiotic mutant some synapsis is directly preceded by a profound nuclear desynaptic2 (dsy2), homologous chromosome pairing and reorganization, generation of the telomere bouquet (Zick- recombination are reduced by ~70% in male meiosis. ler and Kleckner 1998). Although the telomere bouquet Fluorescent in situ hybridization studies demonstrate that has been postulated to facilitate chromosome association a normal telomere bouquet develops but the pairing of a and synapsis by bringing homologous subtelomeric representative gene locus is still only 25%. Chromosome regions into close proximity (Scherthan et al. 1996; Bass synapsis is aberrant as exemplified by unsynapsed regions et al. 1997), this does not explain how homology is of the chromosomes. In the mutant, we observed unusual identified between partner chromosomes within the RAD51 structures during chromosome pairing. Instead of bouquet itself. spherical single and double RAD51 structures, we saw During homologous chromosome synapsis, electron long thin filaments that extended along or around a single microscopy revealed small electron-dense structures be- chromosome or stretched between two widely separated tween chromosomes that were termed early recombina- chromosomes. Mapping with simple sequence repeat tion nodules (RNs) based on their structural similarity to (SSR) markers places the dsy2 gene to near the centro- late RNs (reviewed in Zickler and Kleckner 1998). Late mere on chromosome 5, therefore it is not an allele of RNs have been directly correlated with the occurrence rad51. Thus, the normal dsy2 gene product is required for and distribution of chiasmata and meiotic recombination both homologous chromosome synapsis and proper events (Carpenter 1975). Though the role of early RNs is RAD51 filament behavior when chromosomes pair. still subject to debate, they were predicted to contain recombination enzymes and be involved in a subclass of recombination events, namely gene conversion (Carpenter 1987). The relationship between these early RNs and Introduction recombination-type events has been confirmed, in part, by immunoelectron microscopy. Anderson et al (1997) and Meiosis couples genetic recombination with the segrega- Tarsounas et al. (1999) have demonstrated the presence of tion of homologous chromosomes and is broadly con- RecA homologs (described below) associating specifical- ly with early RNs in lily and in mice. However, it is an open question as to whether or not these early RNs are Edited by: P. Moens converted into late RNs. A. E. Franklin · I. N. Golubovskaya · W. Z. Cande ()) Genetic studies in budding yeast have demonstrated Department of Molecular and Cell Biology, that the eukaryotic RecA homologs, RAD51 and DMC1, 345 Life Sciences Addition, are involved in meiotic recombination (Bishop et al. University of California at Berkeley, 1992; Shinohara et al. 1992). Meiotic recombination is Berkeley, CA 94720, USA e-mail: [email protected] initiated by the introduction of a double-stranded break by the protein SPO11 (Keeney et al. 1997). Single-stranded H. W. Bass 30 DNA tails are created by other proteins, and RAD51 Department of Biological Science, and DMC1 are then loaded onto these 30 single-stranded Florida State University, DNAs where they act to mediate recombination (Rock- Tallahassee, FL 32306–4370, USA 18 mill et al. 1995). In vitro, RAD51 protein can polymerize around a single chromosome or stretched between two onto single-stranded DNA and the resulting nucleoprotein chromosomes. In contrast, normal maize RAD51 zygo- filament can undergo DNA strand invasion into a tene structures are present as small single and double homologous double-stranded DNA target (Baumann et spheres on chromosomes. Therefore, the normal dsy2 al. 1996), so it makes sense that RAD51 is involved in gene product is required for homologous chromosome identification of homologous sequences. synapsis and the normal pattern of RAD51 distribution The relationship between recombination and homolo- during zygotene. gous synapsis is unclear since some organisms require SPO11 for synapsis, and others do not. For example, in mice, it has been demonstrated that SPO11-induced Materials and methods double-stranded breaks (monitored by a unique histone phosphorylation) and the subsequent recruitment of Genetic mapping RAD51/DMC1 to these sites occurs prior to the initiation Genetic mapping of the dsy2 gene was performed using waxy - of synapsis (Mahadevaiah et al. 2001). In other organ- linked translocation chromosomes and translocation B chromo- isms, such as Caenorhabditis elegans (Dernberg et al. somes. For simple sequence repeat (SSR) segregation analysis, the 1998) and Drosophila (McKim and Hayashi-Hagihara dsy2 mutant (parental inbred line A344) was outcrossed to the W23 1998), SPO11 is dispensable for homologous chromo- inbred line and selfed. The tissue samples were collected from 12 F2 dsy2 mutants, and parental W23 and A344 individuals. some synapsis but is still required for meiotic recombi- Polymorphisms between W23 and A344 inbred lines were identi- nation. Thus, we cannot generalize about the relationship fied for chromosome 5 SSR markers p-bnlg1208, located in bin between homologous synapsis and recombination. How- 5.03, p-dupssr10, located in bin 5.04, and p-bnlg1346, located in ever, there may be a relationship between recombination bin 5.07 (see the maize database at http://www.agron.missouri.edu/ and homologous pairing. In mice and maize, while ssr.html for publicly available sequence data for these primers). DNA purification and the polymerase chain reaction (PCR) were chromosomes are pairing in zygotene, numerous performed essentially according to the SSR Method Manual, also at RAD51 foci are present on the unpaired and paired http://www.agron.missouri.edu/ssr.html. The PCR samples were chromosomes, suggesting that some recombination ma- electrophoresed on a 5% polyacrylamide/TAE gel and stained with chinery components may be involved in homolog recog- ethidium bromide to visualize bands. nition (Ashley et al. 1995; Franklin et al. 1999). We have been investigating RAD51 behavior in situ by Light and electron microscopy utilizing three-dimensional immunofluorescence micros- copy. By preserving both nuclear and chromosome For light microscopy a squash technique was used to determine chiasmata frequency and number of bivalents per male metaphase I structure, we have been able to visualize the subnuclear cell in three genotypes: dsy2/dsy2 homozygous mutants (four distribution and morphology of native RAD51 complexes plants); dsy2/+ fertile heterozygous sib plants (two plants); and +/+ in maize meiotic nuclei (Franklin et al. 1999). Maize (Zea parental A344 inbred line plants (two plants). Young tassels with mays, L.) undergoes chiasmate meiosis and shares many anthers in meiotic stages prophase I through tetrads were fixed in features of meiotic chromosome behavior in common freshly mixed Farmer’s solution for 24 h at room temperature. The fixed material was then rinsed three times and stored in 70% with humans and mice. In maize, single and double ethanol at 4C. Anthers at the diakinesis/metaphase I stages were RAD51 foci appear on the chromosomes maximally stained with 2% acetocarmine (Carmine, C1022, Sigma) and (range 100–700 foci per nucleus) during zygotene when chromosomes analyzed by light microscopy. The rod-shaped chromosomes are pairing. When chromosomes are com- bivalents indicative of a single chiasma were clearly distinguishable from the ring-shaped bivalents, which typically contain two or pletely aligned and synapsed during pachytene, the more chiasmata (Golubovskaya 1994). number of RAD51 foci, i.e. approximately 2–3 per For the analysis of female meiosis, young ears of four dsy2 chromosome, is similar to the number of expected mutant plants were fixed according to Golubovskaya and Avalkina reciprocal exchanges between homologs. Based on these (1994), and stained with Feulgen’s Reagent. A total of 119 ovules at different meiotic stages were examined. patterns of RAD51 distribution, it is possible that RAD51 A spreading technique was used for examination of maize is involved in two sequential processes during meiosis, synaptonemal complexes (SCs) in spermatocytes by transmission namely the search for homology during chromosome electron microscopy. Fresh anthers with meiocytes in prophase I pairing and then the actual process of meiotic recombi- stages were identified by light microscopy and used for preparing a nation itself. suspension of meiocytes. Suspensions of whole nuclei were spread on the surface of 0.2 M sucrose solution, fixed by exposure to the We have undertaken genetic and cytological analysis
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