116

To pair or not to pair: chromosome pairing and evolution Graham Moore

Chromosome pairing in wild-type wheat closely resembles

the process in both yeast and Drosophila. The recent

characterisation of a mutant Phi wheat and the observation

that chromosome pairing in the absence of Phi more closely

resembles that of mammals and maize has shed light on the

evolution of chromosome pairing in the cereals.

Addresses John lnnes Centre, Colney, Norwich NR4 7UH, UK; e-mail: Foote@bbsrc.ac.uk

Current Opinion in Plant Biology 1998, 1 :116-l 22

http://biomednet.com/elecref/1369526600100116

0 Current Biology Ltd ISSN 1369-5266

Introduction Reduction in chromosome number and genetic recom- bination during meiosis require the prior association of homologous chror’nosomes (homologues). In different organisms, the reciprocal recognition, alignment and association of homologues (part of the chromosome pairing process) occur either during cell development or during meiotic prophase (1,2], suggesting that there is no single organism which is the model for all the others. Comparison of pairing in different organisms may lead instead to a prediction of the generalised process which may have occurred in the ancestral progenitor, and it may reveal the adaptations made to this process during speciation. This review adopts this approach to determining the evolutionary effects of chromosome pairing mechanisms.

Angiosperms can provide an insight into chromosome pairing. hlore than 50% of angiosperms are polyploid, arising either by multiplication of a basic set of chromo- somes (autopolyploidy) or as a result of combining related, but not completely homologous, genomes (allopolyploidy). The stabilisation of allopolyploids requires a restriction of pairing between the different parental chromosomes related by ancestral homology. There are a number of pairing mutants (for example the wheat PIII mutant) which affect this stabilisation. The study of these mutants can shed light on the processes involved. The stabilisation could be achieved using two approaches. Firstly, the parental chromosomes are already structurally distinct or can become distinct after hybridisation by rapidly rearranging themselves through translocation of chromo- some segments and/or inversions. Secondly, there is an adaptation of the processes of chromosome assortment and alignment. Chromosome evolution in polyploids is likely to be a reflection of both these pairing controls.

Structural discrimination or adaptation? Species revealing structural discrimination of parental chromosomes The genomes of maize, rice, barley, sorghum and wheat now have markedly different genome sizes (as a result of an expansion of repeat sequences) and numbers of chromosomes since their speciation some 60 million years ago. A large number of comparative mapping studies have been undertaken (reviewed in [3,4-l 11). The genes on the rice map can be grouped into sets [12] and these same sets of genes (termed rice linkage segments) also describe the genetic maps of all the chromosomes of barley, foxtail millet, maize, sorghum, sugarcane and wheat [ 131. The ten chromosomes of maize can be divided into two sets of five [l&13]. Thus, the maize genome is possibly derived from the hybridisation of two diploid parents, each contributing five chromosomes with different combinations of rice linkage segments and, therefore, has a tetraploid nature. The diploid nature of the sorghum genome is also revealed [13] by analogy to rice linkage segments, and confirmed recently by detailed mapping in comparison with sugar cane [lo]. Some rice linkage segments in one maize parental chromosome set are inverted with respect to those in sorghum and to the other parental chromosome set [ 131. Many of these inversions involve functional centromeres or sites which align with centromeres in other genomes. This suggests that even ancestral sites may still have some functional activity. The two parental chromosome sets of maize either had major structural differences prior to hybridisation or as a result of hybridisation. In common with maize, the genetic mapping of the polyploids oilseed rape (Brassica t~pus) [ 141 and cotton (Gos~~$ilcm barbadense) [15] demonstrate that homology between their parental chromosomes is restricted mainly to chromosome seg- ments. There is no reason to suppose that the mechanism for controlling homologue recognition in these species will be different from that of maize. These genomes were either structurally distinct before hybridisation or became distinct upon hybridisation. The predominance of rearrangements at the centromere revealed by these studies indicates that centromeres appear to be involved in the process of rearranging genomes [16].

Although the rice linkage segments indicate the general gene content of the regions of different cereal chro- mosomes, selection pressures (such as environmental) may have caused amplification, deletion or inversion of particular regions or loci since their divergence. This has happened in the case of disease resistance genes [17*] and cencromeric regions [16]. An apparent loss of synteny (i.e. genetic loci that are linked together on the same chromosome in different species) occurs in

Chromosome Pairing and evolution Moore 117

the case of disease resistance loci [17*] despite their being flanked by markers which show extensive synteny [18]. This may reflect strong selective pressures on these genes, resulting in extensive rearrangements through amplifications, deletions or recombination events. Studies have yet to show extensive colinearity (genetic loci that lie in the same order on the same chromosome in different species) at the physical level between rice, sorghum and maize and some breakdown down in colinearity at this level has been reported [19,20]. In maize, requirements co discriminate between its two chromosome sets and to stabilise itself as a hybrid seem to have involved some homoeologous recombination events [Zl’] and may have also involved other localisarion rearrangements at the microlevel (Kilobase to Megabase level of genome organisation).

At the physical level extensive marker colinearity has been observed between rice and wheat genomes (including the region defined by the deletion in the wheat PM pairing mutant) [22,23]. A region flanking the Pi2 locus, however, has been subject to many breakage and fusion events [23]. Some markers in this region are associated with centromeric sites in other species. Many centromeric sites seem to be associated with particular gene families, possibly reflecting some functional link. It would be intriguing if the PM locus is flanked by an ancient centromeric site and is thus linked with associated gene families possibly controlling its function.

Importance of centromeres in genome rearrangements In situ hybridisation using probes specific for cen- tromeres and telomeres reveals that, except during meiotic prophase, cereal chromosomes are organised in a Rabl configuration, that is to say with the cencromeres clustered in one hemisphere and telomeres at the other pole [24*]. Cereal chromosomes can naturally break at their centromeres presumably by incorrect attachment of microtubules to both sides of the centromere and then the subsequent pulling on this side in opposite directions. Cereal chromosomes broken next to their centromeres and with a telomere now added at this site have two possible nuclear configurations. Theoretically, both telomeres could be at the telomeric pole (taking the centromere to this pole), or the centromere could be located with the other centromeres at the other pole (taking with it a telomere) [ZS]. The latter situation occurs, thus indicating the dominance of centromeres in determining nuclear organisation. This dominance and clustering may explain the importance of centromeres in rearranging the maize genome and provide the means to achieve it through fusion of centromeres.

Some 80 million years ago cereals (Gramineae), rushes (Juncaceae) and sedges (Cypericeae) diverged from a common ancestor. The chromosomes of rushes and sedges are holocentric (i.e. with a diffuse centromere) possessing many sites along the length for microtubule attachment.

Holocentric chromosomes can naturally fragment to create smaller viable chromosomes [26] and this fragmentation is likely to occur at centromere sites. In hybrids between parental lines carrying the original larger chromosomes and these small fragmented chromosomes, one large chromo- some pairs with several small chromosomes [27]. Clearly these species are very adept at aligning their chromosomes. Segregation of chromosomes in such hybrids could lead to an increase in gene content in the grass family. Thus Gramineae chromosomes may have evolved from a holocentric progenitor and, therefore, possess several potential sites for microtubule attachment.

Recently, a family of conserved sequences (CCSl) located at the centromeres of all rice, maize, wheat, barley and rye chromosomes has been identified [28*]. Certain members of this conserved sequence family also detect telomeric heterochromatin [28*]. The rice linkage segments could be defined by the same family of sequences. In fact CCSl is not the only conserved sequence described as being part of the cereal centromeres. Using in situ hybridisation, Jiang and colleagues [‘29*] described a probe designed to target a specific sequence of repetitive DNA which detected the centromeres of cereals. The level of stringency of this in situ hybridisation suggests that this sequence has diverged more significantly than CCSl in the genomes of these species. It is unclear whether both these sequences are part of the same unit, but CCSl also contains many inverted repeats, one inside another [28’]. The only previously identified repeat to have such a structure was a long-terminal repeat (LTR) found on a retrotransposon [30]. It is possible chat CCSl may not be the sequences specifying the mounting of the kinechore which attach microtubules for chromosome segregation. They may be part of a large block of repetitive DNA located at the centromere (centromeric repeats) which have been conserved for some other function related to centromere involvement in either nuclear organisation or pairing.

Comparison of the centromere sites in the genomes of rice, wheat and maize reveals that the borders of the rice linkage segments are defined by centromeric and telomeric sites [ 161. Telomeric heterochromatin in maize, rye, wheat and Bromus can, under certain conditions, function as neocentromeres (reviewed in [16]) and con- tains CCSl-related sequences. The borders of linkage segments could in fact be defined by centromere-like sites. The generalised genome structure of the ancestral grass can be predicted using the rice linkage segments and creates a single chromosome pair [12]. By breaking this chromosome at centromeric sites and by creating inversions, the two sets of maize chromosomes, the wheat and barley chromosomes, and sorghum and millet chromosomes can all be recreated using the same set of rice segments [13]. The breakage and fusion of rice linkage segments is reminiscent of the evolution of the holocentric chromosomes of rushes and sedges [31]. Thus,

118 Genome studies and molecular genetics

centromeres are involved in determining chromosome organisation in the nucleus and, therefore, in rearranging chromosomes. Are they also involved in chromosome pairing?

Species revealing adaptation of chromosome pairing Hexaploid wheat (n=Zl) is composed of three ancestral genomes or three sets of seven chromosomes. Genetic mapping reveals that the gene order and recombination in- terval is similar between the homoeologous chromosomes [32]. Each chromosome has the potential to pair with five other chromosomes but it pairs only with its homologue. The mechanism controlling pairing in wheat must have been functioning at the time of hybridisation and in contrast to maize did not require a major rearrangement of its chromosomes. Hexaploid wheat has 42 centromeres, but their somatic nuclei have an average of 22 centromeric hybridisation sites located on their nuclear membranes [24*]. Centromeres are located at the nuclear membrane and occur in pairs, although in most cases not with their homologue [33”]. Two loci (P/z2 and P&Z, on chromosomes SB and 3D respectively) have been defined as controlling pairing in hexaploid wheat, of which P/i1 has the major effect. Deletion of the Phi locus allows homoeologous chromosomes to pair [34]. A locus carried by a wild relative of wheat, Aeghps speltoides, can suppress the effect of the P/II locus, thus also allowing homoeologous pairing [35]. All three loci have been shown to affect centromeric heterochromatin structure during premeiotic interphase and meiotic prophase. Thus, it seems that strict homologous pairing is correlated with a tight centromeric heterochromatin structure while homoeologous pairing is correlated with a diffuse structure [24*]. There may be an effect on other heterochromatin sites. Is centromeric heterochromatin involved in chromosome pairing?

Chromosome recognition and association From the random organisation of each homologue in the premeiotic nucleus to their close association at pachytene (i.e. the stage at which crossing over of genetic infor- mation occurs), homologues need to undergo reciprocal recognition, coalignment and synapsis, termed collectively as chromosome pairing. Many methods used to study the process, such as squashing the nucleus before microscopy, either actually disrupt the three-dimensional structures to be observed or make it difficult to determine whether the cells are somatic or germline in origin (L Aragon-Alcaide, A Bevan, G Moore, P Shaw, unpublished data). At the onset of sporulation in yeast, 3550% of the homologues are colocalised and associated [36,37]. At the onset of meiotic prophase DNA replication occurs, resulting in the slight separation of homologues from each other, although they still remain colocalised [36]. The remaining chromosomes are now aligned and associated (Figure 1; [36]).

Using anther sections of up to three cell layers in thickness and confocal microscopy, meiotic pairing of two homologues in wheat has been studied during anther

development (330.1 and confocal microscopy three-dimen- sional reconstructions of chromosomes during anthesis have been made. The following summary of the processes of chromosome pairing in wheat can be produced by combining these data and those studies reviewed by Dover and Riley [38]. At a stage when meiocytes and the surrounding somatic (tapetum) cells cannot visually be distinguished, the homologues are separated. When the meiocytes and tapetum cells are distinguishable, the homologues come in contact at their centromeric repeats in both these cells. This process is colchicine sensitive. The disruption of pre-meiotic spindles by colchicine and non-disruption by chloral hydrate suggested that the control of the meiotic pairing mechanism involved centromeric microtubules of the spindle (not affected by chloral hydrate), which may reflect a sensitivity of the process to increased viscosity within the nucleus. The next step is sensitive to low temperatures which may reflect a sensitivity of the process to increased viscosity within the nucleus. Instead, as in yeast, where only up to 50% of its homologues associate, virtually all the homologues in meiocytes and tapetum cells of wheat now associate [33**]. This is comparable to the process in DrosopMa, and other Dipterans, where up to 90% of homologues associate during embryo development and remain associated until meiocic segregation [39,40]. The wheat centromeres then migrate, the chromosomes decondense and DNA replication then occurs [41,42]. In contrast to the process in yeast, the decondensed homologues appear to remain associated at the start of meiotic prophase. The lack of separation of chromosomes at this stage could reflect either the resolution of the study, some chromosome structure difference or simply that their sheer size in comparison to yeast chromosomes means that, once together, it is more difficult for them to come apart. Equally, the presence of centromeric repeats and centromeric heterochromatin (large blocks of repeats flanking the centromere which in wheat can reflect two thirds of the chromosome arm and are organised in reiterating units; reviewed in [3]) and particular associated proteins in both wheat and Drosoph’a chromosomes may enable homologous chromosomes to efficiently interlock, in contrast to yeast chromosomes which lack centromeric heterochromatin. Whatever the reason, wheat chromosomes are aligned and do not realign again during meiotic prophase.

It has been argued that mammals are ancestral autopoly- ploids [43] whose genomes underwent two rounds of multiplication, followed, as in the case of allopolyploid maize, by rearrangement. Chromosome pairing in both species occurs during meiotic prophase. Mammalian studies performed using sections and light microscopy have indicated that during the pre-meiotic interphase homologues are not in a Rabl configuration (i.e. the centromeres are not clustered in one hemisphere, although telomeres are at the other pole; see Figure 1). This possibly reflects the loss of centromere dominance in determining nuclear organisation during development.

Chromosome pairing and evolution Moore 119

Figure 1

Drosophila and other Dipterans

Wheat (Ph 1 +)

Wheat (Ph 1 -)I Maze

- Centromere dommance p - Telomere dominance c

Pre-meiotic C During embryo development + f

Interphase 4

t Meioiic prophase -

DNA replication cluster switch of

+- Dying floral development -w Up to 90% homoloQu= centromeres to

Sporulation

Up to 90% of homologues

Up to 50% of homologues

(A) Indicates associated

(C) Indicates colocalised

Current Opmn I” Plant Biology

Chromosome pairing in maize resembles the situation occurring in the Phi mutant wheat. The organisation of two homologous chromosomes is shown in the nucleus at various stages, with disks (0) representing centromeres and the lines representing chromosome arms terminating in telomeres. Nuclei containing (?) reflect stages requiring further clarification. Mammalian centromeres cluster just before meiotic prophase,. orientating their chromosomes in a similar configuration (Rabl) to those in maize and the wheat Phi mutant (a line lacking chromsosome 58) at the onset of meiotic prophase.

Just before meiotic prophase, however, the mammalian chromosomes adopt a Rabl configuration. Homologues have little contact during premeiotic interphase [42]. The lack of the Rabl configuration and centromere association is consistent with the lack of conservation of sequences forming centromeric repeats. The homologue recognition, colocalisation and association occurs during meiotic prophase [44]. Confocal microscopy studies on maize anther preparations indicate no contact between heterochromatin knobs during premeiotic interphase [45]. The maize chromosomes colocalise and associate during

meiotic prophase [45]. This association is correlated with the movement, clustering and pairing of telomeres which contrasts with the association of wild-type wheat involving centromere movement and pairing. The maize situation is similar to the PM mutant of hexaploid wheat (a line lacking the 5B chromosome), where sites on the homologues do occasionally come into contact during premeiotic interphase but the homologues do not fully associate ([33**] and Figure 1). There is an apparent failure to colocalise at the initial stage when centromeric repeats come into contact, although in the absence of

120 Genome studies and molecular genetics

Phi (Sears mutant), homologues associate in most cases during meiotic prophase and the line is viable for several generations. It has yet to be confirmed whether, in this mutant, chromosome pairing at meiotic prophase exactly resembles that of maize. The data are consistent with the hypothesis proposed by Feldmann and colleagues [45,46] that centromeres are involved in chromosome pairing in wild-type wheat [46,47]. There was no obvious association of homologues, however, either in somatic tissues or in early differentiation stages of meiocytes or tapetum cells [33**].

At first appearance, these data are inconsistent with the studies of Dvorak and colleagues [48,49*], who found that in the absence of Phf, recombination occurs between a pair of wheat chromosomes composed of combinations of homoeologous and homologous segments, but in the presence of P/l, recombination is restricted to homologous segments even when the centromeres and telomeres are homologous. This study, therefore, implies that cen- tromeres (and telomeres) are not important for homologue recognition and that Phi changes the stringency of homology searching and hence the ability to recombine chromosomes [48,49’]. Looking more closely at the issue of centromere involvement, the 42 wheat centromeres start as 21 pairs, mostly nonhomologous centromere contacts. At present, it is not possible to identify whether these contacts are between non-homologous or homoeologous chromosomes. During early floral development of the wild-type wheat this changes to homologous centromere contacts. Twenty pairs will form which are homologous contacts, leaving the remaining centromeres of the homo- eologous/homologous segmented chromosomes to pair (as in somatic tissues) as a nonhomologous contact. Only those segments homologous for their repeats and genes would associate and hence recombine later.

Revaluating the issue of pairing stringency, pairing and recombination can occur in meiotic prophase between two homoeologous chromosomes of rye grass that differ by up to 50% in their chromosome length [50]. The length difference is accounted for by repetitive sequences. Thus genes are likely to be the object of homology searching process during meiotic prophase. The initiation of floral development in wheat, embryo development in Drosophila or sporulation in yeast results in homologue association. Any disruption of homology between the homologues in Drosophila leads to a failure to pair somatically [38]. There is no observable phenotype asso- ciated with this failure, presumably because chromosomes can also associate during meiotic prophase. In fact an observable phenotype might only be clear in a polyploid situation (e.g. the Phl mutant) as an increase in sterility. This initial chromosomal association could be based on homology of genes and repeats and the association during meiotic prophase of only genes. Thus in wheat carrying P/l virtually all the homologues are associated during premeiotic interphase and do not align again

during meiotic prophase. Without actually requiring a modification to the stringency of homology searching and the enzymes involved, the stringency of pairing is in effect raised. Repetitive families can rapidly evolve in the genomes of closely related species [51]. Thus chromosome segments showing structural differences in their repeats would not associate during premeiotic interphase and recombine later. In fact, in wheat most of these repetitive families are concentrated in the proximal two thirds of the chromosome while the genes are clustered in the distal third, so even if the movement of centromeres at the end of premeiotic interphase resulted in separation of the proximal regions, this would not effect recombination events in the presence of Phl providing the subtelomeric regions remained aligned.

Conclusions In summary, chromosome pairing in the presence of PhZ in hexaploid wheat largely resembles the situation found in Drosophila and yeast; conversely, the P/l mutant resembles the situation in maize and mammals. The comparisons (Figure 1) reveal a clear pattern to the process and adaptations made, and suggest that the effect of the Phl mutant might be an ancestral phenotype. Are mammals Ph mutants? What might the function of Phl be? Premeiotic association depends on sequence homology or rather its maintenance in both repeats and genes; therefore, suppression of the activity (expression and recombination) of repeats must occur to maintain similarity between homologues chromosomes. In small genomes repeats are concentrated in centromere regions [52]. The loss of the Phl effect could activate centromeric repeats, resulting in genome expansion, in particular of centromeric heterochromatin. This is consistent with the observation that the major expansion of the Triticeae (wheat, barley and rye) chromosomes appears not to have occurred through activity of the repetitive sequences per se but through nonrandom amplification of groups of repeats around centromeric regions [3]. In contrast, major expansion of the maize genome seems to have occurred through activity of repeats via retrotransposition events (see Bennetzen, this issue [pp 103-1081). The situation would be analogous to the locus coding for a centromere binding protein, CENP-B, which is involved in both the structural conformation of centromeres and the integrity of repeat sequences contained within them [53*]. The absence of a PM-like effect during evolution may confer the selective advantages of being able to rearrange genomes, create variation and hence speciate. It is intriguing that those diploid species whose genomes are related to the B genome of hexaploid wheat carrying the Phi also possess mechanisms for suppressing its effect (541. Interestingly, in common with Ph genes in wheat, the heterochromatin associated proteins in Drosophda affect heterochromatin structure, chromosome segregation, repeat activity (expression and recombination) and have an increased level of expression during the time when chromosomes are paired somatically [55,56]. The presence

Chromosome pairing and evolution Moore 121

of centromeric repeats and hererochromatin and particular associated proteins in Drosophila and wild-type wheat may provide both chromosome specificity and an efficient association of homologues even when they undergo nuclear organisation. It is not inconceivable that the P/r genes encode for heterochromatin associated proteins.

Acknowledgements The author wishes to thank the following for their work in this area: L Aragon-Alcaide, A Bevan, T Foote, T hliller, S Reader, hl Roberts, P Shaw and J Snape, and T Foote for producing the figure.

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