© 2004 The American Genetic Association
Centromere Dynamics and Chromosome Evolution in Marsupials
From the Department of Molecular and Cell Biology U-2131, University of Connecticut, Storrs, CT 06269-2131 (O'Neill and Metcalfe); and the Department of Biological Sciences, Macquarie University, New South Wales 2109, Australia (Eldridge).
Address correspondence to Rachel O'Neill at the address above, or e-mail: roneill{at}uconnvm.uconn.edu.
 |
Abstract |
|---|
 Top Abstract The Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
The eukaryotic centromere poses an interesting evolutionary paradox: it is a chromatin entity indispensable to precise chromosome segregation in all eukaryotes, yet the DNA at the heart of the centromere is remarkably variable. Its important role of spindle attachment to the kinetochore during meiosis and mitosis notwithstanding, recent studies implicate the centromere as an active player in chromosome evolution and the divergence of species. This is exemplified by centromeric involvement in translocations, fusions, inversions, and centric shifts. Often species are defined karyotypically simply by the position of the centromere on certain chromosomes. Little is known about how the centromere, either as a functioning unit of chromatin or as a specific block of repetitive DNA sequences, acts in the creation of these types of chromosome rearrangements in an evolutionary context. Macropodine marsupials (kangaroos and wallabies) offer unique insights into current theories expositing centromere emergence during karyotypic diversification and speciation.
|
The Chromosome: An Historical Perspective |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
The first description of the process of mitosis and the involvement of chromosomes, or "chromatic nuclear figures," was conducted by the German zoologist, Anton Schneider in 1873 (Zacharias 2001). During the last quarter of the 19th century, Fleming (1879) and Strasburger (1875), whose work collectively founded the field of cytogenetics, described mitotic chromosomes in a remarkable variety of plants and animals. The term "chromosome," however, was not introduced until 1888 by Waldeyer, a German professor of anatomy (Zacharias 2001). Although Gregor Mendel's work had not yet been rediscovered (this occurred in 1900), Weismann proposed his chromosome theory of inheritance in 1887, the tenets of which have all proven to be true (Darlington 1966). Working independently of one another, Sutton (1902) and Boveri (1902) formalized this theory by stating chromosomes were the vehicles on which genes traveled during mitosis. Dobzhansky and Sturtevant's (1938) seminal study classifying the chromosome rearrangements that distinguish two Drosophila species provided a detailed analysis of the molecular basis of species identity through chromosome rearrangement. Their pivotal observations launched decades of study of genome architecture and chromosome change from an evolutionary perspective.
The chromosomes of the bandicoot, described by Brenda in 1906 (Sharman 1961), were the earliest reported karyotype for an Australian marsupial and were among the earliest reported for mammals. By the end of the last century, nearly 70% of all marsupial taxa had been karyotyped (Hayman 1990). Having diverged from eutherian mammals 130–180 million years ago (Archibald 2003), marsupials are ideally situated as comparative models for eutherians and have afforded a raft of insights into mammalian physiology, ecology, evolution, and genetics. The latter part of the 20th century witnessed an explosion of highly informative and exciting research in comparative and functional genomics in this group. Molecular genetics studies in marsupials greatly informed our understanding of mammalian sex determination, sex chromosome evolution, and dosage compensation. Sinclair et al. (1988) were able to narrow the search for the sex-determining gene in mammals by showing that a gene, Zfy, proposed to be the testis determining factor (tdf), was autosomal in the tammar wallaby (Macropus eugenii), and therefore unlikely to be tdf. Extensive mapping of the Y chromosome in the tammar wallaby had shown that the origin of the Y predated the divergence of marsupials from eutherian mammals (Graves 1996). Foster et al. (1992) later showed that the gene Sry, which was eventually proven to be tdf, was Y-linked in both marsupials and eutherians. Marsupial sex chromosomes are thought to more closely represent the ancestral state of sex chromosomes (Graves 1996), lacking a pseudoautosomal region and containing a smaller percentage of DNA of the haploid chromosome complement than that in eutherians. Dosage compensation in marsupials, which is imprinted with only the paternal X inactivated, has also been proposed to be representative of the ancestral state (Ohlsson et al. 2001). Marsupials continue to be informative in studies of the molecular mechanisms and evolution of genomic imprinting (O'Neill et al. 2000).
|
Chromosome Evolution in Australasian Marsupials |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
Comparative cytogenetics in marsupials has also greatly enhanced our understanding of species and chromosome divergence. Marsupial karyotypes show a bimodal distribution, with the majority of species exhibiting either a 2n = 14 or 2n = 22 karyotype (Hayman 1990; Sharman 1974). Some authors have argued that 2n = 14 is the ancestral diploid number (Rofe and Hayman 1985), while others have argued that 2n = 22 is ancestral (Svartman and Vianna-Morgante 1998). Comparative G-banding and chromosome painting indicate that the 2n = 14 karyotype is homologous in several evolutionarily divergent lineages, while the many 2n = 22 complements observed in marsupial taxa are not, suggesting that they are independently derived (Hayman 1977; Rofe and Hayman 1985).
While species diversification in some families of marsupial mammals has been accompanied by little karyotypic evolution (the 49 species of dasyurids, for example, all carry a modified 2n = 14 karyotype) (Rofe and Hayman 1985; Young et al. 1982), the Macropodidae (kangaroos, wallabies, and rat-kangaroos) have experienced a recent and explosive radiation of chromosome evolution. It is estimated this group diverged approximately 24 million years ago (Kirsch et al. 1997) and includes 66 species and 14 genera with diploid numbers ranging from 2n = 10/11 (X/Y1Y2) in the Wallabia bicolor (swamp wallaby) to 2n = 32 in the Aepyprymnus rufescens (rufous bettong) (Hayman 1990; Sharman 1961). A 2n = 22 complement, derived from the 2n = 14 ancestral karyotype primarily through five fissions, a centric fusion, centric shifts, and inversions (Rens et al. 1999; Rofe 1979), is considered ancestral to the macropodines (kangaroos and wallabies), and possibly to all Macropodidae (macropodines and rat-kangaroos) (Figure 1) (Eldridge and Close 1993; Hayman et al. 1987; Johnston et al. 1983; Rofe 1978). This ancestral complement, with several derivations, is retained in several lineages, including Thylogale (pademelons), Petrogale (rock wallabies), and Setonix brachyurus (quokka) (Eldridge and Close 1993; Glas et al. 1999; Hayman 1990; Rofe 1978; Sharman 1961).
|
The karyotypic divergence in macropodines is characterized by three types of rearrangements, all involving the centromere: centric fusions (Robertsonian translocations), centric shifts (centromere repositioning within a chromosome in the absence of syntenic gene order rearrangement), and pericentric inversions. These rearrangements are particularly prevalent within two recently derived (5–8 million years ago) genera, Macropus (14 species including W. bicolor) and Petrogale (21 species, subspecies, and races), together representing more than 50% of macropodine taxa. Four suites of centric fusion chromosomes have been identified within Macropus (Rofe 1978). For example, Macropus giganteus (grey kangaroo) and Macropus eugenii (tammar wallaby) share a 2n = 16 diploid number, yet the fusions responsible for three metacentric chromosomes are different. Macropus species and W. bicolor share a number of fusion chromosomes, however, W. bicolor represents the extreme, with seven fusions resulting in a highly derived karyotype with a multiple sex chromosome system (Rofe 1978). When mapped along a phylogeny based on DNA–DNA hybridization (Kirsch et al. 1995), it is clear that the chromosome evolution in this group is complex, with multiple rearrangements in each lineage (Figure 2).
|
With the exception of two subspecies, all 21 taxa within the genus Petrogale exhibit distinct chromosomal complements (Sharman et al. 1990). Inversions, centric fusions, and centric shifts are characteristic of the majority of Petrogale taxa (see Eldridge and Close [1993] for a review). It was found through extensive G-banding studies that inversions were not responsible for the apparent mobility of the centromeres of this genus, but that the centromere location had shifted relative to the ancestral state (Eldridge and Close 1993).
Virtually every species within macropodines carries an X chromosome with the centromere or the X-linked nucleolar organizer region (NOR) in a different location. It has been hypothesized that centric shifts and inversions have been involved in the formation of this diversity of X chromosome morphology (Hayman 1990; Rofe 1979). The prevalence of chromosome changes delineated by a change in genomic architecture involving the centromere within these marsupial lineages suggests this functioning region of the chromosome is a key component in chromosomal divergence.
|
Centromeres and Chromosome Evolution |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
It has been known for quite some time that satellite DNA families can be species and/or group specific (e.g., the alpha satellites of primates) (Singer 1982). However, their seemingly ubiquitous presence at or near centromeric domains across a wide variety of organisms implies they play a role in centromere function (see Eichler [1999], Eichler and Sankoff [2003], Henikoff et al. [2001], and Willard [1990] for reviews). The vast majority of centromere-associated sequences that have been identified to date have included arrays of repeated DNAs (Choo 2000; Sullivan 2001). The notable exception to this includes Saccharomyces cerevisiae, in which the centromere is defined as a "point" centromere that consists of only about 125 bp of DNA (Clarke 1990). This simple structure appears to be a characteristic unique to this species, as other fungal species carry arrays of repeats within their centromeres typical of most eukaryotes (see Cambareri et al. [1998] for an example).
The paradox that centromere function is highly conserved while its sequence structure is highly divergent between taxa has led several authors to speculate on the mechanics of repeated satellite DNA in primary centromere determination (Eichler 1999; Eichler and Sankoff 2003; Henikoff et al. 2001; Willard 1990). The lack of conservation of short sequences across most eukaryotes examined argues against a defined sequence-specific function in determining centromere activity. An alternate proposal suggests that centromere functionality might be epigenetically determined by a higher-order structure dictated by underlying repeats (reviewed in Karpen and Allshire [1997]). Csink and Henikoff (1998) propose that sequence content is irrelevant, but that an ability to evade detrimental sequence insertion (such as mobile element transposition) is necessary. The authors suggest this may be accomplished through an expansion of satellite blocks, providing a spacer or buffer of satellite sequences.
Studies in simian cell lines transfected with human alpha satellite sequences showed that these repetitive regions could form de novo centromeres on existing chromosomes (Haaf et al. 1992). However, later studies characterizing neocentromeric DNA in dicentric chromosomes showed that classical human alpha satellites are not the essential element dictating centromere location in humans (Barry et al. 1999; du Sart et al. 1997). Concordantly, Williams et al. (1998) showed that neocentromeres in Drosophila do not contain classical repeated DNA sequences. Thus, while satellite DNA is linked to centromere function, it is not required (Csink and Henikoff 1998; Willard 1990).
|
Centromere Mobility and Neocentromerization |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
Recently Ventura et al. (2001) showed that the centromere location on the X chromosome in lemurs experienced mobility during species divergence. Using a comparative mapping approach, these researchers were able to show that the linear order of genes on the X chromosomes of the black lemur and ring-tailed lemur has remained conserved during speciation. The centromere of this chromosome, however, has moved in the ring-tailed lemur, resulting in the change from a telocentric to a metacentric chromosome. This type of centric shift has also been characterized in bovids (Iannuzzi et al. 2000), where the X chromosomes of the river buffalo and cattle shared a linear ordering of genes, yet one was acrocentric and the other metacentric, respectively. This shift was also accompanied by a loss of heterochromatin in the metacentric chromosome.
Centromere mobility in karyotypic evolution may be the result of several different factors. A centric shift would seem to require three breaks in the chromosome to move the centromeric block of DNA to another position without disrupting the isosequential order of DNA. This has been regarded as unlikely given the divergence of centromeric sequences between the two X chromosomes in the lemur case (Ventura et al. 2001). It is clear from this study that the ring-tailed lemur X centromere is derived from sequences novel to the X chromosome in this species through a process of de novo centromere emergence (Ventura et al. 2001; Wong and Choo 2001).
Two other theories (Ventura et al. 2001; Wong and Choo 2001) may explain the appearance of new centromeres in a karyotype. The weak cross hybridization of X-linked centromeric sequences isolated from the derived metacentric chromosome in the ring-tailed lemur to centromeres of other chromosomes raises the possibility that this new centromere may have resulted from a transposition or duplication of sequences from another chromosome. It is also possible that centromere emergence has occurred through the co-opting of local sequences to act as the functional centromere or through the reactivation of an ancestral centromere location (Malik and Henikoff 2002). This neocentromerization may be facilitated by modification of local DNA through epigenetic means, such as the deposition of centromere DNA-binding proteins (Choo 2000), changes in the chemical structure of local DNA and bound histones (i.e., methylation, acetylation), or through heterochromatization (Malik et al. 2002).
Blocks of satellite DNA throughout the chromosome may provide substrates for novel modifications and neocentromerization. There is increasing evidence from humans that chromosomes may carry hotspots for neocentromere formation, as in the derivation of centromeres in HSA 13q32 (Warburton et al. 2000). These neocentromeres indicate that centromere competence is a native component of DNA at locations other than the active centromere (Wong and Choo 2001). Centromeres may shift to expanding satellite blocks elsewhere on the chromosome if those blocks become the last region to replicate (Csink and Henikoff 1998).
The link to heterochromatin as a substrate, and possible stabilizer, in centromere formation and function (Henikoff et al. 2000) is intriguing in light of the studies in cattle and in macropodines. The centromere shift in cattle has been accompanied by an apparent loss of heterochromatin. Likewise, the centric shifts in Petrogale are associated with species whose chromosomes carry very small amounts of heterochromatin (Metcalfe et al. 1997; Sharman et al. 1990). Conversely, species within the Macropus group, in which no centric shifts have been identified, carry extensive centromeric heterochromatin (Rofe 1979). Perhaps the lack of heterochromatin in species of Petrogale provides multiple sites of potential neocentromerization while extensive heterochromatin in centrically stable species "locks" the centromere position in place. A causative or associative effect between heterochromatin and centric shifts cannot be determined until the nature of the shift, by derivation of a new centromere or transposition of other centromeric DNAs, has been fully characterized in these groups.
|
Centric Fusions |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
Sequences at the centromere may also play a role in the evolution of new karyotypes through fusions, as has been observed in the cytotypic races of Mus musculus domesticus. More than 40 parapatric races of this species have been identified that display approximately 100 different Robertsonian (Rb) translocations (Nachman et al. 1994). Garagna et al. (2001) have posited that this explosion in karyotypic diversity has been engendered by the activity of minor satellite DNA at the centromere. Analyses of fusion points within Rb chromosomes show that the breakpoints lie within these satellites. It has been proposed that the activity of the centromeric DNA binding protein CENP-B facilitates these types of rearrangements (Garagna et al. 2001; Kipling and Warburton 1997). This protein shares sequence similarity with the pogo family of transposable elements (Tudor et al. 1992) and may promote recombination through its putative ability to nick DNA adjacent to CENP-B boxes within these minor satellite repeats.
In some groups, however, fusion events also result in the retention of subtelomeric and/or telomeric sequences at the site of fusion (Lee et al. 1993). In Petrogale, telomeric sequence is consistently retained near fusion points in centric fusions (Metcalfe et al. 1997). Telomeric and subtelomeric regions of the genome are predisposed to instability. This is evident in the array of segmental duplications and the subsequent fusion responsible for the evolution of human chromosome 2 (Eichler 1999; Fan et al. 2002; Mefford and Trask 2002).
|
Centromeres and Karyotypic Evolution |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
Henikoff and coworkers (Henikoff et al. 2001; Henikoff and Malik 2002; Malik and Henikoff 2002) have proposed that the centromere is a selfish entity, citing as evidence the extremely rapid evolution of centromeric satellites that is tracked by positive directional selection of the centromeric histone H3 variant, cenH3 (Malik and Henikoff 2002; Talbert et al. 2002) in several organisms. The rapid evolution is envisioned as an arms race between selfish DNA elements capable of distorting chromosome segregation (in female meiosis) in their favor, while cenH3 is selected to maintain equal segregation. The characterization of centromeric DNA as comprised of active, selfish genetic elements contradicts other hypotheses that envision the recruitment of centromeres from otherwise inert satellite sequences dispersed throughout genomes (Ventura et al. 2001; Wichmann et al. 1991; Wong and Choo 2001).
It is unclear whether the centromere plays an active role, for example, through its action as a meiotic driver (Henikoff and Malik 2002; Pardo-Manuel de Villena and Sapienza 2001a–c), or a passive role, providing sites for recombination (Kipling and Warburton 1997) and segmental duplications (Eichler 1999) in chromosome evolution. Data from interspecific marsupial hybrids, however, indicates that the centromere does contribute to chromosome diversity and can undergo dramatic shifts in architecture in a short evolutionary time period (i.e., one generation). In a hybrid between two macropodine species, it was found that a retroviral sequence located at the centromere had undergone demethylation and amplification, resulting in chromosome remodeling in this animal (O'Neill et al. 1998). Subsequent analyses of several other macropodine hybrids utilizing cross-species chromosome painting showed that the rearrangements observed in these genomes were restricted to centromeres (O'Neill et al. 2001). These rearrangements may be the result of interchromosomal segmental duplications of centromeric sequences, nonallelic recombination between sequences at those locales, or transposition of mobile DNA or other repeated DNAs. Such a dramatic increase in de novo chromosome rearrangements in these hybrids suggests that a reorganization of the karyotype can occur rapidly (O'Neill et al. 2001).
The underlying cause of the increased instability in these hybrids is unclear. However, there is an intriguing link between parentally derived chromosome heterozygosity and the incidence of hybridization-induced chromosome rearrangements observed in macropodine hybrids. The more divergent the karyotypic morphology of the parental species in any given interspecies cross in this group, the higher the incidence of de novo rearrangements within the resulting hybrid offspring (Figure 3). This positive correlation may be due to an increase in genomic instability produced by hybridization (Fontdevila 1992).
|
Pardo-Manuel de Villena and Sapienza (2001a) have hypothesized that female meiosis, due to its asymmetric nature (Pardo-Manuel de Villena and Sapienza 2001b), drives karyotypic evolution in mammals toward a karyotype that is either all metacentric or all acrocentric, with selection against a heteromorphic karyotype. In humans, it has been found that Robertsonian fusions are transmitted at a higher frequency to the oocyte than their acrocentric partners (Pardo-Manuel de Villena and Sapienza 2001c), while in mice the reverse is true (Pardo-Manuel de Villena and Sapienza 2001a). This drive may be the product of "centromere drive" (Henikoff and Malik 2002), in which the centromeric sequences are diverging rapidly in concert with the divergence of the centromere histone H3 variant. In such a scenario, mixed karyotypes may suffer from an uneven "attraction" between chromosomes for the kinetochore machinery. Reorganization of centromeric sequences in macropodine hybrids may be the result of such a drive. While centromere repositioning was not observed in these hybrids, the apparent translocation of centromeric sequences indicates that interchromosomal centromere transposition does occur. Likewise, the cross-hybridization signals observed in these centromeres may be the result of duplication and homogenization events (Eichler 1999), a process that, to date, has only been identified in mouse and human (Thomas et al. 2003). The dramatic changes observed in marsupial hybrids involving epigenetic modification and centromere restructuring may reflect events important during the divergence of new karyotypes.
|
Acknowledgments |
|---|
We thank M. J. O'Neill for editorial comments and helpful discussion regarding this manuscript. This work is supported by National Science Foundation grant NSF-0093250 (to R.J.O.). M.D.B. Eldridge is supported by the Australian Research Council (QEII Fellow). This paper was originally presented at the American Genetics Association 2003 Annual Meeting and Centennial Celebration at the University of Connecticut, Storrs, July 18–30, 2003.
|
Footnotes |
|---|
Corresponding Editor: Kent E. Holsinger
|
References |
|---|
|
TopAbstractThe Chromosome: An Historical...Chromosome Evolution in...Centromeres and Chromosome...Centromere Mobility and...Centric FusionsCentromeres and Karyotypic...References |
|---|
-
Archibald DJ, 2003. Timing and biogeography of the eutherian radiation: fossils and molecules compared. Mol Phylogenet Evol. 28:350-359.[CrossRef][Web of Science][Medline]
Barry AE, Howman EV, Cancilla MR, Saffery R, Choo KH, 1999. Sequence analysis of an 80 kb human neocentromere. Hum Mol Genet. 8:217-227.
Boveri T, 1902. Über mehrpolige Mitosen als Mittel zur Analyse des Zellkerns. Verh phys-med Ges. 35:67-90.
Cambareri EB, Aisner R, Carbon J, 1998. Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats. Mol Cell Biol. 18:5465-5477.
Choo KHA, 2000. Centromerization. Trends Cell Biol. 10:182-188.[CrossRef][Web of Science][Medline]
Clarke L, 1990. Centromeres of budding and fission yeasts. Trends Genet. 6:150-154.[CrossRef][Web of Science][Medline]
Csink AK, Henikoff S, 1998. Something from nothing: the evolution and utility of satellite repeats. Trends Genet. 14:200-204.[CrossRef][Web of Science][Medline]
Darlington C, 1966. The chromosomes as we see them. In: Chromosomes today, vol. 1 (Lewis K, ed). Edinburgh: Oliver and Boyd; 1–6.
Dobzhansky T, Sturtevant AH, 1938. Inversions in the chromosomes of Drosophila pseudoobscura. Genetics. 23:28-64.
du Sart D, Cancilla MR, Earle E, Mao J, Saffery R, Tainton KM, Kalitsis P, Martyn J, Barry AE, Choo KHA, 1997. A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat Genet. 16:144-153.[CrossRef][Web of Science][Medline]
Eichler EE, 1999. Repetitive conundrums of centromere structure and function. Hum Mol Genet. 8:151-155.
Eichler EE, Sankoff D, 2003. Structural dynamics of eukaryotic chromosome evolution. Science. 301:793-797.
Eldridge MDB, Close RL, 1993. Radiation of chromosome shuffles. Curr Opin Genet Dev. 3:915-922.[CrossRef][Medline]
Fan Y, Linardopoulou E, Friedman C, Williams E, Trask BJ, 2002. Genomic structure and evolution of the ancestral chromosome fusion site in 2q13-2q14.1 and paralogous regions on other human chromosomes. Genome Res. 12:1651-1662.
Fleming W, 1879. Beiträge zur Kenntnis der Zelle und ihrer Lebenser-scheinungen I. Arch Mikrosk Anat. 16:302-346.
Fontdevila A, 1992. Genetic instability and rapid speciation: are they coupled? Genetica. 86:247-258.[CrossRef]
Foster JW, Brennan FE, Hampikian GK, Goodfellow PN, Sinclair AH, Lovell-Badge R, Selwood L, Renfree MB, Cooper DW, Graves JA, 1992. Evolution of sex determination and the Y chromosome: SRY-related sequences in marsupials. Nature. 359:531-533.[CrossRef][Medline]
Garagna S, Marziliano N, Zuccotti M, Searle JB, Capanna E, Redi CA, 2001. Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci USA. 98:171-175.
Glas R, De Leo AA, Delbridge ML, Reid K, Ferguson-Smith MA, O'Brien PCM, Westerman M, Graves JAM, 1999. Chromosome painting in marsupials: genome conservation in the kangaroo family. Chromosome Res. 7:167-176.[CrossRef][Web of Science][Medline]
Graves JA, 1996. Mammals that break the rules: genetics of marsupials and monotremes. Annu Rev Genet. 30:233-260.[CrossRef][Web of Science][Medline]
Haaf T, Warburton PE, Huntington FW, 1992. Integration of human a-satellite DNA into simian chromosomes: centromere protein binding and disruption of normal chromosome segregation. Cell. 70:681-696.[CrossRef][Web of Science][Medline]
Hayman DL, 1977. Chromosome number – constancy and variation. In: The biology of marsupials (Stonehouse B and Gilmore D, eds). London: Macmillan; 27–48.
Hayman DL, 1990. Marsupial cytogenetics. Aust J Zool. 37:331-349.[CrossRef]
Hayman DL, Rofe RH, Sharp PJ, 1987. Chromosome evolution in marsupials. Chromosomes Today. 9:91-102.
Henikoff S, Ahmad K, Malik HS, 2001. The centromere paradox: stable inheritance with rapidly evolving DNA. Science. 293:1098-1102.
Henikoff S, Ahmad K, Platero JS, van Steensel B, 2000. Heterochromatic deposition of centromeric histone H3-like proteins. Proc Natl Acad Sci USA. 97:716-721.
Henikoff S, Malik HS, 2002. Centromeres: selfish drivers. Nature. 417:227.[CrossRef][Medline]
Iannuzzi L, Di Meo GP, Perucatti A, Incarnato D, Schibler L, Cribiu EP, 2000. Comparative FISH mapping of bovid X chromosomes reveals homologies and divergences between the subfamilies bovinae and caprinae. Cytogenet Cell Genet. 89:171-176.[CrossRef][Web of Science][Medline]
Johnston PG, Davey RJ, Seebeck JH, 1983. Chromosome homologies in Potorous tridactylus and P. longipes (Marsupialia: Macropodidae) based on G-banding patterns. Aust J Zool. 32:319-324.[CrossRef]
Karpen GH, Allshire RC, 1997. The case for epigenetic effects on centromere identity and function. Trends Genet. 13:489-496.[CrossRef][Web of Science][Medline]
Kipling D, Warburton PE, 1997. Centromeres, CENP-B and Tigger too. Trends Genet. 13:141-145.[CrossRef][Web of Science][Medline]
Kirsch JAW, Lapointe F-J, Foeste A, 1995. Resolution of portions of the kangaroo phylogeny (Marsupialia: Macropodidae) using DNA hybridization. Biol J Linn Soc Lond. 55:309-328.
Kirsch JAW, Lapointe F-J, Springer MS, 1997. DNA-hybridisation studies of marsupials and their implications for metatherian classification. Aust J Zool. 45:211-280.[CrossRef]
Lee C, Sasi R, Lin CC, 1993. Interstitial localization of telomeric DNA sequences in the Indian muntjac chromosomes: further evidence for tandem chromosome fusions in the karyotypic evolution of the Asian muntjacs. Cytogenet Cell Genet. 63:156-159.[Web of Science][Medline]
Malik HS, Henikoff S, 2002. Conflict begets complexity: the evolution of centromeres. Curr Opin Genet Dev. 12:711-718.[CrossRef][Web of Science][Medline]
Malik HS, Vermaak D, Henikoff S, 2002. Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone. Proc Natl Acad Sci USA. 99:1449-1454.
Mefford HC, Trask BJ, 2002. The complex structure and dynamic evolution of human subtelomeres. Nat Rev Genet. 3:91-102.[CrossRef][Web of Science][Medline]
Metcalfe CJ, Eldridge MDB, McQuade LR, Johnston PG, 1997. Mapping the distribution of the telomeric sequence (T2AG3)n in rock-wallabies, Petrogale (Marsupialia: Macropodidae), by fluorescence in situ hybridization. I. The penicillata complex. Cytogenet Cell Genet. 78:74-80.[Web of Science][Medline]
Nachman MW, Boyer SN, Searle JB, Aquadro CF, 1994. Mitochondrial DNA variation and the evolution of Robertsonian chromosomal races of house mice, Mus domesticus. Genetics. 136:1105-1120.[Abstract]
O'Neill MJ, Ingram RS, Vrana PB, Tilghman SM, 2000. Allelic expression of IGF2 in marsupials and birds. Dev Genes Evol. 210:18-20.[CrossRef][Web of Science][Medline]
O'Neill RJ, Eldridge MDB, Graves JAM, 2001. Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids. Mamm Genome. 12:256-259.[CrossRef][Web of Science][Medline]
O'Neill RJ, O'Neill MJ, Marshall Graves JA, 1998. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature. 393:68-72.[CrossRef][Medline]
Ohlsson R, Paldi A, Graves JA, 2001. Did genomic imprinting and X chromosome inactivation arise from stochastic expression? Trends Genet. 17:136-41.[CrossRef][Web of Science][Medline]
Pardo-Manuel de Villena F, Sapienza C, 2001a. Female meiosis drives karyotypic evolution in mammals. Genetics. 159:1179-1189.
Pardo-Manuel de Villena F, Sapienza C, 2001b. Nonrandom segregation during meiosis: the unfairness of females. Mamm Genome. 12:331-339.[CrossRef][Web of Science][Medline]
Pardo-Manuel de Villena F, Sapienza C, 2001c. Transmission ratio distortion in offspring of heterozygous female carriers of Robertsonian translocations. Hum Genet. 108:31-36.[CrossRef][Web of Science][Medline]
Rens W, O'Brien PCM, Yang F, Graves JAM, Ferguson-Smith MA, 1999. Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosome Res. 7:461-474.[CrossRef][Web of Science][Medline]
Rens W, O'Brien PC, Fairclough H, Harman L, Graves JA, Ferguson-Smith MA, 2003. Reversal and convergence in marsupial chromosome evolution. Cytogenet Genome Res. 102:282-290.[CrossRef][Web of Science][Medline]
Rofe R, Hayman D, 1985. G-banding evidence for a conserved complement in the Marsupialia. Cytogenet Cell Genet. 39:40-50.[Web of Science][Medline]
Rofe RH, 1978. G-banded chromosomes and the evolution of the Macropodidae. Aust Mamm. 2:53-63.
Rofe RH, 1979. G-banding and chromosomal evolution in the marsupials (PhD dissertation). Adelaide, Australia: University of Adelaide.
Sharman GB, 1961. The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust J Zool. 9:38-60.
Sharman GB, 1974. Marsupial taxonomy and phylogeny. Aust Mamm. 1:137-154.
Sharman GB, Close RL, Maynes GM, 1990. Chromosome evolution, phylogeny and speciation of rock wallabies (Petrogale: Macropodidae). Aust J Zool. 37:351-363.[CrossRef]
Sinclair AH, Foster JW, Spencer JA, Page DC, Palmer M, Goodfellow PN, Graves JA, 1988. Sequences homologous to ZFY, a candidate human sex-determining gene, are autosomal in marsupials. Nature. 336:780-783.[CrossRef][Medline]
Singer MF, 1982. Highly repeated sequences in mammalian genomes. Int Rev Cytol. 76:67-112.[Web of Science][Medline]
Strasburger EA, 1875. Zellbildung und Zellteilung. Jena, Germany: Fischer.
Sullivan KF, 2001. A solid foundation: functional specialization of centromeric chromatin. Curr Opin Genet Dev. 11:182-188.[CrossRef][Web of Science][Medline]
Sutton WS, 1902. On the morphology of the chromosome group in Bachystola magna. Biol Bull. 4:24-39.
Svartman M, Vianna-Morgante AM, 1998. Karyotype evolution of marsupials: from higher to lower diploid numbers. Cytogenet Cell Genet. 82:263-266.[CrossRef][Web of Science][Medline]
Talbert PB, Masuelli R, Tyagi AP, Comai L, Henikoff S, 2002. Centromeric localization and adaptive evolution of an Arabidopsis histone H3 variant. Plant Cell. 14:1053-1066.
Thomas JW, Schueler MG, Summers TJ, Blakesley RW, McDowell JC, Thomas PJ, Idol JR, Maduro VV, Lee-Lin SQ, Touchman JW, Bouffard GG, Beckstrom-Sternberg SM, Green ED, 2003. Pericentromeric duplications in the laboratory mouse. Genome Res. 13:55-63.
Tudor M, Lobocka M, Goodell M, Pettitt J, O'Hare K, 1992. The pogo transposable element family of Drosophila melanogaster. Mol Gen Genet. 232:126-134.[CrossRef][Web of Science][Medline]
Ventura M, Archidiacono N, Rocchi M, 2001. Centromere emergence in evolution. Genome Res. 11:595-599.
Warburton PE, Dolled M, Mahmood R, Alonso A, Li S, Naritomi K, Tohma T, Nagai T, Hasegawa T, Ohashi H, Govaerts LC, Eussen BH, Van Hemel JO, Lozzio C, Schwartz S, Dowhanick-Morrissette JJ, Spinner NB, Rivera H, Crolla JA, Yu C, Warburton D, 2000. Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere. Am J Hum Genet. 66:1794-1806.[CrossRef][Web of Science][Medline]
Wichmann HA, Payne CT, Ryder OA, Hamilton MJ, Maltbie M, Baker RJ, 1991. Genomic distribution of heterochromatic sequences in equids: implications to rapid chromosomal evolution. J Hered. 82:369-377.
Willard HF, 1990. Centromeres of mammalian chromosomes. Trends Genet. 6:410-416.[CrossRef][Web of Science][Medline]
Williams BC, Murphy TD, Goldberg ML, Karpen GH, 1998. Neocentromere activity of structurally acentric mini-chromosomes in Drosophila. Nat Genet. 18:30-37.[CrossRef][Web of Science][Medline]
Wong LH, Choo AKH, 2001. Centromere on the move. Genome Res. 11:513-516.
Young GJ, Marshall Graves JA, Barbieri I, Woolley PA, Cooper DW, Westerman M, 1982. The chromosomes of dasyurids (Marsupialia). In: Carnivorous marsupials (Archer M, eds). Sydney, Australia: Royal Zoological Society of New South Wales; 783–795.
Zacharias H, 2001. Key word: chromosome. Chromosome Res. 9:345-355.[CrossRef][Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  C. J. Metcalfe, K. V. Bulazel, G. C. Ferreri, E. Schroeder-Reiter, G. Wanner, W. Rens, C. Obergfell, M. D. B. Eldridge, and R. J. O'Neill Genomic Instability Within Centromeres of Interspecific Marsupial Hybrids Genetics, December 1, 2007; 177(4): 2507 - 2517. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Bulazel, C. Metcalfe, G. C. Ferreri, J. Yu, M. D. B. Eldridge, and R. J. O'Neill Cytogenetic and Molecular Evaluation of Centromere-Associated DNA Sequences From a Marsupial (Macropodidae: Macropus rufogriseus) X Chromosome Genetics, February 1, 2006; 172(2): 1129 - 1137. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. E. Holsinger From Genes to Genomes: The Next Century of Heredity in America J. Hered., September 1, 2004; 95(5): 363 - 364. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||