Department of Molecular and Cell Biology, University of California Berkeley, 345 LSA 3200, Berkeley, CA 94720-3200, USA
* Author for correspondence (e-mail: zcande{at}berkeley.edu)
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Summary |
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Key words: Meiosis, Telomere clustering, Bouquet, Chromosome pairing, Synapsis
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Introduction |
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We make a distinction between chromosome pairing and chromosome synapsis. By pairing, we mean whatever processes are used to bring chromosomes into co-alignment and to search base pairs for homology. Synapsis is a separate process and involves installation of the central element of the synatonemal complex (SC), which glues the two homologs together along their lengths. We know pairing and synapsis are separate events because homology is not required for synapsis (Pawlowski et al., 2004).
The mechanism of telomere clustering and the molecules needed to bring it about have remained obscure partly because it has not been possible to observe telomere clustering in living cells and few mutants exist that would aid in the identification of proteins associated with the bouquet. However, progress has been made through analysis of bouquet formation in mutant meiocytes in several model organisms, including maize, mouse, and budding and fission yeast. Below, we discuss results from studies that suggest that bouquet formation is an active process, as well as review evidence indicating that the function of the meiotic bouquet is actually to make meiotic prophase much faster and more efficient.
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The bouquet in context |
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In maize, at the leptotene-zygotene transition, there is an abrupt shift in telomere and centromere behavior. Before zygotene, centromeres are confined to one nuclear hemisphere; afterwards, they have no obvious nuclear organization. Telomeres behave the opposite way: prior to zygotene there is no observable polarity; afterwards the telomeres are both polarized and clustered on the NE (Carlton and Cande, 2002). In this context, polarized means that centromeres and/or telomeres localize to one hemisphere of the nucleus. At the leptotene-zygotene transition, this shift is caught in the act', such that most telomeres lie in one nuclear hemisphere and most centromeres lie in the other (because this is difficult to see in flat projections, the reader is encouraged to see the supplemental movies, http://jcs.biologists.org/supplemental/). Similar dramatic changes in polarity have been described in other organisms. For example, in fission yeast, centromeres are normally clustered near the spindle pole body (SPB) in haploid cells, and telomeres are loosely grouped at the other end of the nucleus; as cells mate and nuclei fuse and meiosis begins, the telomeres cluster at the SPB and the centromeres are released (Chikashige et al., 1997
). The polarization switch in maize coincides with the transient elongation of large blocks of heterochromatin called knobs and of centromeric heterochromatin, which is consistent with the notion that the large-scale changes in nuclear organization might be mediated by changes at a lower-order level of chromatin organization (Carlton and Cande, 2002
).
The meiotic bouquet is readily visualized at the light microscope level in many organisms, in which one can follow the path of the condensed threadlike zygotene chromosomes within the nucleus (Scherthan, 2001). In some organisms, including maize, visualization of the bouquet is difficult in squashes, where chromosome orientation is perturbed. In other organisms such as yeast (Trelles-Sticken et al., 1999
) and Arabidopsis (Armstrong et al., 2001
), the bouquet can be seen in chromosome squashes. However, fluorescent in situ hybridization (FISH) using telomere and centromere probes, together with 3D reconstructions of nuclei imaged by deconvolution or confocal laser scanning fluorescence microscopy, have rendered the analysis of the bouquet much easier. In addition, transmission electron microscopy (TEM) has shown that, in metazoans and plants, attachment plaques form on the inside of the NE just before the bouquet stage and the axial elements that form the lateral elements of the SCs appear to insert into the plaques (Fig. 2). These structures move closer together as the bouquet forms. The proteins involved in forming this attachment are not known. Although mouse spermatocytes lacking the SC protein SCP3 lack axial elements and conical thickenings, telomeres are still attached to the inner NE through an electron-dense plate that contains telomere DNA repeats and several cohesins (Liebe et al., 2004
).
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The meiotic bouquet and the Rabl arrangement |
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Rules of telomere behavior revealed by studying chromosome derivatives |
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The mechanism of bouquet formation |
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What drives the polar movement of telomeres? In algae and animals, the centrosome is found directly outside the NE, adjacent to the telomere cluster (Scherthan, 2001). In fission yeast, telomeres form a tight cluster on the NE adjacent to the SPB, which is not yet inserted into the NE (Chikashige et al., 1994
). These observations have led to the suggestion that cytoplasmic microtubules interacting with components in the NE drive telomere clustering, but there is no evidence that confirms this model. It is equally plausible that the centrosome is attracted to the bouquet site on the NE. Higher plants do not have obvious microtubule-organizing centers (MTOCs), and depolymerization of cytoplasmic microtubules by vinblastine and amiprophos-methyl (APM), a plant herbicide, does not inhibit telomere clustering in meiocytes in rye anther culture. This suggests that the telomere clustering is not dependent on cytoplasmic microtubules in plants (Cowan and Cande, 2002
).
Interestingly, colchicine blocks bouquet formation in plants at low concentrations that do not depolymerize the cytoplasmic microtubule arrays. Although colchicine is a well-studied microtubule-depolymerizing drug, it also affects the function of other proteins, including at least one transmembrane protein (reviewed by Cowan and Cande, 2002). Addition of colchicine to rye anthers in culture at various times during prophase I (leptotene through pachytene) specifically disrupts the lateral movement of telomeres on the NE but does not affect other nuclear reorganizations, such as nuclear pore rearrangement (Cowan and Cande, 2002
). When applied to plants and animals early in meiotic prophase, colchicine causes improper synapsis, decreased chiasmata formation and a greatly reduced frequency of recombination, yielding univalent chromosomes followed by infertility (Loidl, 1990
; Zickler and Kleckner, 1998
). In higher plants and mice, the leptotene-zygotene transition may be the most colchicine-sensitive stage: treatment with colchicine after zygotene has no effect on meiosis (Loidl, 1990
). Since colchicine blocks telomere clustering in the rye system, and disrupts homologous synapsis in many other cell types, the two processes might be causally related.
A remaining question concerns the identity of the colchicine-sensitive target. Notably, inhibition of bouquet formation in rye anthers treated with colchicine is very similar to the block in bouquet formation in pam1 mutant maize meiocytes, which also exhibit aberrant synapsis (see below); thus, it is possible that cloning of the pam1 gene will shed light on this target. We speculate that the bouquet-specific colchicine target is an as-yet-unidentified cytoskeletal component that is associated with the inner face of the NE. The drug studies discussed above demonstrate that the mechanism responsible for generating the chromosomal movements associated with bouquet formation are autonomous to the nucleus and do not appear to rely on the cytoplasmic cytoskeleton.
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The bouquet in fission yeast plays an important role in homologous chromosome alignment |
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Bouquet dissolution is highly regulated |
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Bouquet function: what does it do? |
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Perhaps the best way to determine the function of the bouquet is to analyze the phenotype of mutants that cannot make a bouquet. There are now such bouquet initiation mutants from several organisms, but deduction of bouquet function is complicated by the fact that many meiotic mutants have mild bouquet problems in addition to other larger problems. Defining mutants whose primary lesion is the inability to create a bouquet is difficult, and thus deducing the bouquets normal function remains problematic. In maize, several mutants have a mild telomere-clustering aberration - for example, phs1 (Pawlowski et al., 2004) and dsy1 (Bass et al., 2003
) - yet have severe defects either in pairing and recombination or in synapsis. In our opinion, there are two mutants that appear to have problems in bouquet formation as their primary defect: pam1 in maize and ndj/tam1 in budding yeast.
As its name implies, the pam1 mutant of maize has plural abnormalities of meiosis. Golubovskaya et al. found that telomeres attach normally to the NE, and are normally polarized in the nucleus (Golubovskaya et al., 2002). They undergo some initial stages of clustering by making several small clumps of telomeres (similar to those seen in rye anthers treated with colchicine), but cannot cluster into a normal tight bouquet. This is the earliest observable defect found in the pam1 mutants because leptotene looks completely normal under both deconvolution 3D microscopy and TEM. Mutant pam1 meiotic nuclei also have aberrant synapsis including nonhomologous synapsis, partner switches and foldbacks, and loss of interlock resolution. There is also a dramatic reduction in homologous pairing (which can be monitored by determining the location of 5SrRNA loci in pachytene nuclei). In addition, there is an extreme asynchrony of meiosis such that, in old anthers that would normally contain only pollen (the product of two post-meiotic mitotic divisions), meiocytes are found in all stages of meiosis from zygotene to the tetrad stage. This could be due to arrest of meiocytes at various points along the meiotic cell cycle, or it could be due to a slowing down of meiotic events. The pam1 mutant is male sterile and almost completely female sterile; however, a few female meiocytes (<1%) do complete normal meiosis. This suggests that formation of a bouquet in maize greatly facilitates pairing, synapsis and resolution of interlocks, but is not absolutely required for these processes, because some meiocytes can ultimately produce normal gametes.
What is the effect on recombination in the pam1 mutant? Interestingly, RAD51 foci on zygotene chromosomes look completely normal, which suggests that the early stages of recombination do not require bouquet initiation and that these two processes can be separated. The converse has also been shown (formation of the bouquet does not require initiation of recombination): spo11 mutants in yeast and Sordaria, which lack recombination, make fine bouquets (Storlazzi et al., 2003; Trelles-Sticken et al., 1999
). This implies that initation of the bouquet and of recombination are independent events.
In the budding yeast bouquet mutant ndj/tam1 (Chua and Roeder, 1997; Conrad et al., 1997
; Trelles-Sticken et al., 2000
), telomeres do not attach to the NE, as they do in the wild type, and thus telomeres cannot cluster opposite the SPB. This indicates that attachment to the NE is required for bouquet formation. Ndj1p localizes to telomeres and probably facilitates attachment to the NE; however, it has not been shown to be part of the attachment plaque. The phenotype of the ndj mutant is surprisingly similar to that in the pam1 maize mutant; there is a severe delay of the onset and completion of synapsis, an extreme delay in all stages of meiotic prophase, non-homologous synapsis, decreased homologous pairing (monitored by FISH), and some sterility. Interestingly, chromosome condensation is not effected in either pam1 or ndj, and thus condensation is probably not related to the bouquet.
Given the similarity of phenotypes of the maize pam1 and yeast ndj/tam1 mutants, we propose that the bouquet is required for efficient homologous pairing and synapsis. The bouquet is not absolutely required for pairing (because the pam1 and ndj mutants do achieve some homologous pairing), for synapsis (again, both mutants can achieve some degree of synapsis), or for completion of meiosis (in both mutants there are always some survivors). However, the rate and efficiency of all these processes are severely reduced in these bouquet mutants. We can also conclude that the bouquet is required for timely initiation of synapsis because synapsis is severely delayed in both the pam1 mutant and the yeast ndj mutant. Analysis of the phenotype of phs1 mutants, which synapse at the normal time and place, albeit non-homologously, demonstrates that homologous pairing is not required for synapsis. So, the bouquet might affect these two processes in different manners.
Regarding the contribution of the bouquet to recombination, our view is that the initial stages of recombination - double-strand breaks, followed by DNA strand invasion facilitated by RAD51 and DMC1 - contribute more to homologous pairing than does the bouquet. However, it is likely that the bouquet, and the movements associated with it (such as in the Schizosaccharomyces pombe horsetail), is required to bring the chromosomes into close enough proximity for strand invasion. The bouquet could almost be evolutionarily dispensable because mutants and colchicine-treated meiocytes are not 100% sterile; some exceptional meiocytes are able to complete normal meiosis. This is in contrast to mutants that, for example, have a disrupted homology search, such as phs in maize (Pawlowski et al., 2004), or are unable to synapse at all, such as zip1 in yeast (Sym et al., 1993
). Meiosis in these mutants is never completed. Moreover, C. elegans and Drosophila lack a bouquet yet are able to complete meiosis (McKee, 2004
), and in other organisms, such as Sordaria (Tesse et al., 2003
) and polyploid wheat (Aragon-Alcaide et al., 1997
), homologs have already found each other by the time the bouquet has formed.
One simple model of how the bouquet could act in meiosis can be proposed. At leptotene or the leptotene-zygotene transition, recombination is initiated by the generation of double-strand breaks, which are resected and then loaded with RAD51 and other proteins. Concurrently and independently, the telomeres, which have attached to the NE earlier in leptotene, cluster first in small clumps, and then into a tight bouquet. Following this, RAD51-coated single-strand DNA overhangs begin to search for homology, which we speculate begins at the chromosome ends. Synapsis follows closely, also starting from the chromosome ends, but does not require a signal that homology has been established. Exit from the bouquet stage probably does require a signal from the recombination pathway [perhaps upon completion of the noncrossover (Allers and Lichten, 2001) recombination pathway], and possibly from the synapsis process. When pairing and synapsis are complete, and recombination is well underway, the telomeres exit the bouquet stage. This is followed by further condensation, SC breakdown and chiasmata maturation, all leading to the uniquely meiotic separation of homologous chromosomes at anaphase 1.
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Concluding remarks |
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Acknowledgments |
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Footnotes |
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