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* Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut 06269, Cambridge Resource Centre for Comparative Genomics, Department of Clinical Veterinary Medicine, University of Cambridge, Cambridge CB2 1TN, United Kingdom, Department Biologie I, Ludwig-Maximilians-Universität München, 80638 Munich, Germany and Australian Museum, Sydney, New South Wales 2010, Australia
2 Corresponding author: Department of Molecular and Cell Biology, U-2131, 354 Mansfield Rd., Room 323, University of Connecticut, Storrs, CT 06269.
E-mail: rachel.oneill{at}uconn.edu
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The family Macropodidae exhibits recent and extensive chromosome evolution, in contrast with most other marsupials, which are generally karyotypically conservative (reviewed in HAYMAN 1990; ELDRIDGE and METCALFE 2006). Chromosome evolution within macropodids has been extensively studied; the majority of macropodids have been karyotyped and the evolutionary trajectory of chromosome rearrangements has been determined (HAYMAN 1990; ELDRIDGE and CLOSE 1993; BULAZEL et al. 2007). Within the genus Macropus (kangaroos and wallabies), rearrangements involving the centromere predominate, in particular centric fusions (ROFE 1978; HAYMAN 1990) and whole-arm reciprocal translocations (WARTs) (reviewed in O'NEILL et al. 2004). However, the mechanism responsible for the rapid karyotypic diversification within this group of mammals has not been fully explored.
Instances of rapid genomic change can result from an increased mutation rate caused by genome destabilizing events, such as inter- and/or intraspecific hybridization or exposure to environmental mutagens and stress (FONTDEVILA 1992). This increase in mutation rate has been observed to coincide with an increase in the local activity of transposable elements, retroelements, and other repeated DNAs (see LIM and SIMMONS 1994; O'NEILL et al. 1998; LABRADOR et al. 1999; FONTDEVILA 2005; UNGERER et al. 2006). In addition to a bias in sequence classes involved in rearrangement, extensive genome sequence comparisons and comparative cytogenetics now point to specific chromosome features, such as centromeres, that can also influence the number, position, and type of rearrangement.
Our previous work in macropodid hybrids showed that a retroviral sequence located at the centromere had undergone demethylation and amplification, concomitant with chromosome remodeling (O'NEILL et al. 1998). Subsequent analyses using cross-species chromosome painting of four other macropodid hybrid individuals (hybrids) showed that the rearrangements observed in these genomes were also restricted to centromeres (O'NEILL et al. 2001).
In our previous work, it was not determined whether the observed rearrangements were shared in other hybrids of the same type or whether the rearrangements were the result of interchromosomal segmental duplications of centromeric sequences, non-allelic recombination between sequences at centromeres on different chromosomes, or whether they resulted from the transposition and/or amplification of mobile DNA or other repeated DNAs. In this study, the genomes of four interspecific hybrids from a cross between two macropodid species not previously studied, Macropus rufogriseus (maternal component) and Macropus agilis (paternal component), were assayed for chromosome rearrangements and genomic instability using standard cytological staining techniques, cross-species chromosome painting, DNA probe analyses, as well as ultrastructural analyses of centromeres via scanning electron microscopy.
These data show that the centromere is a significant contributing factor in chromosome aberration in all of the hybrid genomes examined. The current analyses show that, in these hybrids, some centromeres differ structurally from parental chromosomes and are the site of extensive genome rearrangements accompanied by DNA amplification of retroelement sequences and satellites. These rearrangements include a broad array of abnormalities typical of genomic instability, including fissions, isochromosomes, whole-arm reciprocal translocations, and minichromosomes. Remarkably, rearrangements were found only within the maternal complement and all were associated with the maternally derived centromeres. This study extends previous work and, for the first time, clearly defines the centromere as the site of genomic instability, anomalous chromosome structures, and structural variants.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Three normal parental animals (A1843, R1188, and R3242) were examined. The male M. agilis (A1843) is the father of all hybrids. The M. rufogriseus animal, R1188, is the mother of RA1188. The mother of the remaining hybrids is from the same population as R1188 but could not be identified by microsatellite analysis (data not shown). An unrelated M. rufogriseus male (R3242) was also examined.
Cell culture:
Ear biopsies were obtained from animals held at Macquarie University, Fauna Park. Primary fibroblast cultures were established from ear biopsies and maintained using standard techniques (COOPER et al. 1977). Cultures were passaged no more than 10 times, with the exception of R3242 (>15 passages). Metaphases were prepared using standard techniques from all cultures. Cytogenetic techniques were performed on metaphases from the three parental animals (A1843, R1188, and R3242) and four hybrids (RA1190, RA1122, RA1188, and "new" RA).
C-banding:
Metaphases from each species were C banded using the technique of SUMNER (1972) as modified by ELDRIDGE (1991).
Scanning electron microscopy:
Chromosomes were isolated according to the "drop/cryo" technique (for details see MARTIN et al. 1994). Briefly, cell suspensions as per standard chromosome preparations were dropped onto cold laser-marked slides (Laser Marking, Fischen, Germany). Just prior to fixative evaporation, 20 µl of 45% acetic acid was applied, and the specimens were covered with a cover slip and frozen upside down on dry ice for 15 min. The cover slip was pried off, and specimens were immediately transferred into fixative (2.5% glutaraldehyde, 75 mM cacodylate buffer, 2 mM MgCl2, pH 7.0).
For DNA staining, chromosomes were incubated for 30 min at room temperature with platinum blue ([CH3CN]2Pt oligomer, 10 mM, pH 7.2) and washed with distilled water and then with 100% acetone prior to critical point drying (for details see WANNER and FORMANEK 1995).
Specimens were washed in distilled water, dehydrated in 100% acetone, and critical point dried from CO2. Slides were mounted onto stubs and carbon coated by evaporation. Specimens were examined at accelerating voltages from 15 to 30 kV with an Hitachi S-4100 field emission scanning electron microscope equipped with a yttrium aluminum garnet (YAG)-type backscattered electron (BSE) detector (Autrata). Secondary electron and BSE images were recorded simultaneously with Digiscan hardware (Gatan).
Preparation of chromosome paints and fluorescence in situ hybridization:
Flow sorting and chromosome paint production of Petrogale xanthopus (2n = 22 karyotype) chromosome paints were performed according to the protocol previously described (RENS et al. 1999). Highly pure chromosome samples were collected, with the exception of the Y chromosome, which was too small to be collected. Pools of individually isolated chromosome DNA were subjected to degenerate oligo primed (DOP)–PCR amplification for incorporation of either biotin– or digoxigenin (DIG)–dUTP (Roche) as per the manufacturer's instructions. Cross-species chromosome painting was performed as described by O'NEILL et al. (1999) with the following modifications. P. xanthopus genomic DNA was sonicated to between 200 and 500 bp and was used for suppression during a preannealing step prior to hybridization. Biotin-labeled probes were detected using avidin–fluorescein-5-isothiocyanate (FITC) (Vector Labs) and digoxigenin probes were detected with antidigoxigenin rhodamine (Roche). Metaphases were captured on an Olympus AX70 microscope equipped with a Photometrics Sensys CCD camera and analyzed using the Genus Cytovision software (Applied Imaging).
Five chromosome paint "sets" were used corresponding to P. xanthopus chromosomes 1 and 10; 6, 9, and 7; 5 and 8; 3 and 4; and 2 and the X chromosome. The five paint sets correspond to M. rufogriseus and M. agilis chromosomes 1p and 1q; 6p, 6q and 7; 3p and 3q; 4 and 5; and chromosome 2 and the X chromosome, respectively. A total of 3094 metaphases were scored, 376–479 for each parent and hybrid individual. Cross-species chromosome painting was also performed and subject to analysis on an unrelated M. rufogriseus male to determine if observed hybrid-specific rearrangements were found within the parental species.
Dot-blot analyses of sat23 and KERV:
Dot-blot analyses were performed on each parent and hybrid animal, and serial dilutions of DNA concentrations ranging from 500 to 0.005 ng/µl were denatured for 5 min at 99°, snap cooled, and spotted onto Hybond N+ (Amersham, Piscataway, NJ) membrane and fixed according to the manufacturer's protocol. Blots were prehybridized and hybridized according to FERRERI et al. (2005) at 65° overnight, washed in 1x SSC, 0.1% SDS at 65°, and exposed to film overnight at –80°. Cytb probe was produced by PCR as per BULAZEL et al. (2007) and hybridized as for sat23 and KERV.
Fluorescence in situ hybridization (sat23 and KERV):
The sat23 (pGEM-T vector containing 1.5 copies of the 178-bp satellite) and KERV-1 (pGEM-T vector containing 1.5 kb spanning the gag-pro-pol region of the retrovirus) probes were labeled with biotin–dUTP and digoxigenin–dUTP, respectively, through PCR amplification of insert DNA using 100 ng each of the plasmid primers SP6 and T7. PCR products were cleaned with a microcon 100, and 2 µl (of 10 µl) was resuspended in 8 µl of hybridization buffer (50% formamide, 10% dextran sulfate, 50 mM Na2HP04, 2x SSC) and denatured at 80° for 10 min. Following denaturation in 70% formamide/2x SSC at 70° for 2 min and processing through a serial ethanol series at –20°, slides were hybridized in the presence of probe overnight at 37°. For metaphases from hybrids, post-hybridization washes were performed as per BULAZEL et al. (2006). For metaphases from M. agilis, low-stringency post-hybridization washes (three washes of 50% formamide/2x SSC for 5 min each; three washes of 2x SSC for 5 min each) were performed at room temperature. The biotinylated probe was detected with antibiotin rhodamine (Molecular Probes, Eugene, OR) and DIG-labeled probe was detected with FITC-anti-DIG antibody (Molecular Probes). Metaphases were counter stained with 4',6-diamidino-2-phenylindole (DAPI). Images were captured as described above.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Four hybrids produced from a cross between M. agilis and M. rufogriseus were confirmed as interspecific offspring on the basis of cytological examination of chromosome complements. In each case, the maternal and paternal complements are readily identifiable by X chromosome morphology differences and the marked centromere length differences for all chromosomes (LOWRY et al. 1995; BULAZEL et al. 2006).
Previous studies of marsupial hybrids indicated a predominance of centromere-associated rearrangements within macropodid hybrids (O'NEILL et al. 1998, 2001). To examine gross constitutive heterochromatin amounts at the centromeres of hybrids in this study, C-banding was performed. C-banding is a technique that specifically stains blocks of constitutive heterochromatin, typically at centromere locations. C-banding patterns (dark-staining regions) are markedly different between each parental animal (Figure 1, A–C), with extensive centromeric heterochromatin in M. rufogriseus and little detectable centromeric heterochromatin in M. agilis. The origin of each homologous chromosome in the hybrids was clearly identifiable by its C-banding pattern; the M. rufogriseus-derived autosomes within the hybrids are clearly identified as the chromosomes with extended, dark-staining centromere regions.
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To test for a correlation between the copy numbers of these two centromere-predominant sequences and the abnormally extended centromeres observed within the hybrid genomes, dot-blot analyses were performed to assay for copy-number variance in relation to the parent from which the maternal complement was derived (M. rufogriseus). The titration dilution used in this assay was necessarily low due to the extreme high copy number of these sequences at the centromeres within M. rufogriseus (BULAZEL et al. 2006) compared with M. agilis. Thus, as M. agilis carries both KERV-1 and sat23 at its centromeres in significantly lower copy number than M. rufogriseus (BULAZEL et al. 2006, 2007), all copies in the former species were essentially diluted to nondetectable levels in this assay. Dot-blot hybridization levels were normalized with cytB and intensities were examined on the Bio-Rad (Hercules, CA) Gel Doc EQ, Quantity One software package. Table 1 shows that each hybrid exhibited an average approximately twofold increase over the M. rufogriseus parent in copy number of both sat23 and KERV-1 sequences.
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Cross-species chromosome painting:
To test whether there were other structural abnormalities present within the karyotypes of these hybrids, cross-species chromosome painting was performed using two-color fluorescence in situ hybridization and dual-peak localization of chromosome paints derived from P. xanthopus. This species was used for cross-species analyses as it carries the ancestral macropodid karyotype (ELDRIDGE et al. 1991, 1992). Each paint probe was used in a two-probe hybridization to delineate de novo rearrangements in each parent, each of the four hybrids, and an unrelated male M. rufogriseus cell line that had undergone a high number of passages.
No rearrangements for any chromosome paint pair were observed in either of the two parental animals or in the unrelated M. rufogriseus male (Table 2A). In contrast, each hybrid carried a mosaic suite of rearrangements at varying frequencies (Table 2B), with most rearrangements classified as unique (Table 2C). Table 2 lists the frequency of each observed rearrangement by chromosome paint pair. A 
2 test was used to determine whether the number of rearrangements observed in the hybrids was statistically significant. The number of rearrangements was found to be significantly different in hybrids compared with the parents (2 = 21, d.f. = 1, P = 3.214 x 10–6). The M. rufogriseus-derived chromosome in the hybrids was easily identified both by inverse DAPI, where the M. rufogriseus chromosome showed extensive staining at the centromere, and by a lack of hybridization of the chromosome paints at the M. rufogriseus-derived centromere. Each of the observed rearrangements in the hybrids involved the M. rufogriseus-derived centromere and included isochromosomes, WARTs, and fissions (Figure 6). However, each hybrid cell line was mosaic for cells with abnormal chromosomes derived from independent rearrangement events (i.e., de novo for each cell) and karyotypically normal cells. While only one tissue (fibroblast) was available for this study, this level of mosaicism within one tissue type implies that the instability may manifest late in development and is likely continuing at a low frequency.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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The increased frequency of chromosome rearrangements in these hybrids is specific only to the centromere that within the parental species (M. rufgogriseus) contains higher copy numbers of both centromeric sequences, sat23 and KERV, as determined by fluorescence in situ hybridization (FISH) (BULAZEL et al. 2006, 2007) (Figure 5) and dot-blot analyses (Table 1). These rearrangements consist of a broad spectrum of karyotypic instabilities, including WARTs, fissions, isochromosomes, and minichromosomes. FISH localization of both the KERV-1 element and the sat23 satellite repeat suggests that, in the hybrids, amplification has occurred at the M. rufogriseus-derived centromere, supporting the SEM data. The amplification of KERV-1 in all four of these hybrids is analogous to that previously observed in another macropodid hybrid (O'NEILL et al. 1998) and implies a general mechanism for genomic instability involving retroelement amplification in marsupial hybrid karyotypic instability specific to centromere locations.
Transposable elements (TEs) have been shown to be directly responsible for chromosome rearrangements in both plants and insects (ZHANG and PETERSON 1999; EVGEN'EV et al. 2000; CACERES et al. 2001). In Drosophila, for example, there is a high correlation between the presence of a particular TE and chromosome rearrangements (LIM 1988; EVGEN'EV et al. 2000). A more detailed study of genome rearrangements in maize showed that a duplication/deletion event can be produced by a single transposition event involving a full-length TE and a TE fragment (ZHANG and PETERSON 1999). However, there are fewer examples of direct involvement of TEs in mammalian genome remodeling. Inversions in primates are known to be induced by recombination of some transposable elements (SCHWARTZ et al. 1998; KEHRER-SAWATZKI et al. 2002). Gerbils of the genus Taterillus have undergone rapid and extensive chromosome repatterning with concomitant amplification of LINE-1 elements. A clear lack of correlation between LINE-1 accumulation and chromosomal breakpoints, however, suggests that these elements were not directly involved in the chromosomal changes (DOBIGNY et al. 2004). The authors suggest that during intense genome repatterning some epigenetic features, such as DNA methylation, are relaxed, allowing TE amplification (DOBIGNY et al. 2004). The amplified KERV-1 element at the hybrid centromere may therefore be directly involved in the various chromosome rearrangements observed or, alternatively, the chromosome rearrangements observed may be concomitant with genomic stress during which epigenetic controls, such as DNA methylation or histone modification, are relaxed. In the Macropus hybrids, it is unclear whether epigenetic restructuring of the centromere allowed the KERV-1 and repeat amplification observed or whether the amplifications resulted in chromatin remodeling.
Hybrid centromeres are structurally modified:
Knobs were first described in maize by MCCLINTOCK 1929). In maize, they appear in pachytene cells as darkly staining heterochromatic regions at intercalary positions and are composed of repeat elements and retrotransposable elements (ANANIEV et al. 1998). Knobs represent a structural manifestation in meiosis of these chromosomal elements. In rice, a correlation has been observed between the size of the knob and the amount of repeat DNA, suggesting that a minimum amount of tandemly repeated DNA may be required to induce knob-like heterochromatic structure that can be visualized by microscopic methods (CHENG et al. 2001). In plants, centromeres are characterized by extremely large blocks of tandem repeats and retrotransposons (HOUBEN AND SCHUBERT 2003). It is interesting that, in this respect, the centromeres of these marsupial species and their hybrids resemble plant chromosomes. To our knowledge, however, there are no reports of elongated or "segmented" plant centromeres.
The observed segmented or "knob-like" structures in mitotic metaphase chromosomes at the M. rufogriseus-derived centromeres in the hybrids were visible within elongated centromeres and not consistently found in the same position on a particular chromosome. This may indicate that the instability at these centromeric loci is not fixed but is in a dynamic state of chromatin remodeling. Three-dimensional ultrastructural analysis shows that, although these centromeres do not contain "knobs" in the dimension suggested by light microscopic data, they not only are elongated with respect to other chromosomes in their complement, but also are characterized by more chromomeres and a denser chromatin configuration with respect to other plant and animal mitotic centromeres (WANNER and FORMANEK 1995, 2000; SUMNER 1998). Similar centromere elongations in human chromosomes have been described for cases of cytosine hypomethylation such as observed with 5-azacytidine (methylase antagonist) treatment and ICF (immunodeficiency, centromeric instability, and facial abnormalities) syndrome (SUMNER 2003; MINIOU et al. 1994) and have been attributed to decondensation of centromeric heterochromatin. Our results showing that the elongated hybrid centromeres are DNA rich support an amplification event rather than a decondensation event. ISH and dot-blot analysis confirm that the elongated centromeres are indeed manifestations of a significant increase in DNA repeats. Further immunodetection experiments are necessary to determine the degree of methylation in the hybrid centromeres.
Centromere evolution and hybrid dysgenesis:
Recent observations with regards to the rapid evolution of a centromeric protein in plants and animals (MALIK and HENIKOFF 2001; TALBERT et al. 2004) suggest that genomic conflict in the form of centromere drive (HENIKOFF et al. 2001; HENIKOFF and MALIK 2002; MALIK and HENIKOFF 2002) may be responsible for the centromere instability at the M. rufogriseus-derived centromeres. Centromere protein C (CENP-C) is a large protein that binds to vertebrate centromeric DNA (SUGIMOTO et al. 1994) with low sequence conservation except for a CENP-C motif (TALBERT et al. 2004). The observation that both centromeres and CENP-C are rapidly evolving (TALBERT et al. 2004), even between closely related species, suggests that a disconnect between CENP-C and centromeric sequence between the two parental centromeres may be responsible for the centromere instability observed in the marsupial hybrids (O'NEILL et al. 1998, 2001; this study). However, it is not clear why this instability should be confined to the M. rufogriseus-derived centromere.
The most obvious difference between the M. rufogriseus and M. agilis karyotypes is the difference in the amount of constitutive heterochromatin at the centromeres, as evidenced by C-banding. The large amounts of heterochromatin at the M. rufogriseus centromeres may be the result of past centromeric drive activity. TALBERT et al. (2004) propose a centromeric drive model, based on karyotypic drive in female meiosis (PARDO-MANUEL DE VILLENA and SAPIENZA 2001), to explain the apparent anomaly of rapidly evolving sequence but conserved function in centromeres and centromeric proteins. They suggest that, because only one product of female meiosis ends up in the final meiotic product, centromeres "compete" during female meiosis. A centromere that is "stronger" will have a greater chance of ending up in the single female meiotic product. However, differences in centromeric drive in male meiosis, where all products end up in the final meiotic product, may result in reduced male fertility. Mutations in CENP-C that restore centromere parity in male meiosis will therefore be selected for in males. Recurrent cycles of selection for "stronger" centromeres in females and "restoring" CENP-C in males would result in the observed rapid evolution of CENP-C and centromeres (TALBERT et al. 2004). They further suggest that addition of satellite repeats at the centromere would attract more centromere histones (CenH3 or CENP-A), thus binding more microtubules during cell division and creating a "stronger" centromere (TALBERT et al. 2004).
Genome repatterning in the four marsupial hybrids is limited to the M. rufogriseus centromere and correlates with the presence of the larger amounts of heterochromatin at these locations. Previous studies indicated that large heterochromatic blocks at centromeres of this species contain CENP-B-binding sequences. However, these centromeres do not form a large kinetochore region spread across these heterochromatic sequences, but, contrary to the centromere drive model, form a small, confined kinetochore akin to that of species with small centromere regions (BULAZEL et al. 2006). The apparent restructuring of chromatin fibers at hybrid M. rufogriseus centromeres may be indicative of more extensive remodeling at these loci, although kinetochore size and CENP-A affinity have not been assayed. However, one backcross hybrid has been previously examined (LOWRY et al. 1995), the karyotype of which did not indicate preferential inheritance of the M. rufogriseus-derived centromere.
An alternative hypothesis for the chromatin remodeling and destabilization of these centromeres is that there is an incompatibility within the RNA interference (RNAi) machinery. RNA silencing or RNA interference occurs in a wide variety of eukaryotic organisms (MEISTER and TUSCHL 2004) and is involved in gene regulation, transposable element mobilization suppression, and epigenetic regulation of heterochromatin. RNA interference appears to be involved in the regulation of centromere function and architecture, in particular with the epigenetic maintenance of heterochromatic regions (GREWAL and JIA 2007). While it has been better studied in yeast (VOLPE et al. 2002, 2003) and Drosophila (PAL-BHADRA et al. 2004), there is evidence that RNAi is also involved in maintenance of heterochromatic and centromeric regions in mammals (FUKAGAWA et al. 2004; KANELLOPOULOU et al. 2005; BOUZINBA-SEGARD et al. 2006). It has been proposed that incompatibility between short interfering RNAs (LIPPMAN and MARTIENSSEN 2004) or piwi-interacting RNAs (BRENNECKE et al. 2007) between maternal and paternal species within a hybrid genome may lead to transposon activation and/or disruption of heterochromatic structure and ultimately to hybrid dysgenesis. Such activation could lead to copy-number increases and chromosome instability, as well as chromatin remodeling, all features of our hybrid system. The difference seen between M. rufogriseus- and M. agilis-derived centromeres may simply be an effect of a larger region in M. rufogriseus in which disruption of epigenetic maintenance could occur.
Conclusions:
Here we have identified centromeric instability and remodeling in hybrids within a marsupial genus known for rapid chromosome evolution predominately involving centromere-involved rearrangements. We observed the same instability in all four hybrids, which was confined to the maternally derived centromeres containing large blocks of heterochromatin that are expanded relative to the paternally derived centromere. The inherent instability that we have identified in this region of the genome may have a role in the rapid chromosome evolution and speciation within macropodids.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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ANANIEV, E. V., R. L. PHILLIPS and H. W. RINES, 1998 A knob-associated tandem repeat in maize capable of forming fold-back DNA segments: Are chromosome knobs megatransposons? Proc. Natl. Acad. Sci. USA 95: 10785–10790.
BOUZINBA-SEGARD, H., A. GUAIS and C. FRANCASTEL, 2006 Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc. Natl. Acad. Sci. USA 103: 8709–8714.
BRENNECKE, J., A. A. ARAVIN, A. STARK, M. DUS, M. KELLIS et al., 2007 Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089–1103.[CrossRef][Medline]
BULAZEL, K., C. METCALFE, G. FERRERI, J. YU, M. ELDRIDGE et al., 2006 Cytogenetic and molecular evaluation of centromere-associated DNA sequences from a marsupial (Macropodidae: Macropus rufogriseus) X chromosome. Genetics 172: 1129–1137.
BULAZEL, K. V., G. C. FERRERI, M. D. ELDRIDGE and R. J. O'NEILL, 2007 Species-specific shifts in centromere sequence composition are coincident with break point reuse in karyotypically divergent lineages. Genome Biol. 8: R170.[CrossRef][Medline]
CACERES, M., M. PUIG and A. RUIZ, 2001 Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions. Genome Res. 11: 1353–1364.
CHENG, Z., R. M. STUPAR, M. GU and J. JIANG, 2001 A tandemly repeated DNA sequence is associated with both knob-like heterochromatin and a highly decondensed structure in the meiotic pachytene chromosomes of rice. Chromosoma 110: 24–31.[Medline]
COOPER, D. W., C. EDWARDS, E. JAMES, G. B. SHARMAN, J. L. VANDEBERG et al., 1977 Studies on metatherian sex chromosomes. VI. A third state of an X-linked gene: partial activity for the paternally derived Pgk-A allele in cultured fibroblasts of Macropus giganteus and M. parryi. Aust. J. Biol. Sci. 30: 431–443.
DOBIGNY, G., C. OZOUF-COSTAZ, P. D. WATERS, C. BONILLO, J. P. COUTANCEAU et al., 2004 LINE-1 amplification accompanies explosive genome repatterning in rodents. Chromosome Res. 12: 787–793.[CrossRef][Medline]
DUTRILLAUX, B., 1979 Chromosomal evolution in primates: tentative phylogeny from Microcebus murinus (Prosimian) to man. Hum. Genet. 48: 251–314.[CrossRef][Medline]
ELDRIDGE, M. D. B., 1991 Chromosomal rearrangements and speciation in rock wallabies, Petrogale. Ph.D. Thesis, Macquarie University, Sydney.
ELDRIDGE, M. D. B., and R. L. CLOSE, 1993 Radiation of chromosome shuffles. Curr. Opin. Genet. Dev. 3: 915–922.[CrossRef][Medline]
ELDRIDGE, M. D. B., and C. J. METCALFE, 2006 Marsupial chromosomes, pp. 9–62 in Atlas of Mammalian Chromosomes, edited by S. J. O'BRIEN, J. MENNINGER and W. NASH. Wiley, New York.
ELDRIDGE, M. D. B., R. L. CLOSE and P. G. JOHNSTON, 1991 Chromosomal rearrangements in rock wallabies Petrogale (Marsupialia: Macropodidae). IV. G-banding analysis of the Petrogale lateralis complex. Aust. J. Zool. 39: 621–628.[CrossRef]
ELDRIDGE, M. D. B., P. G. JOHNSTON and R. L. CLOSE, 1992 Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia: Macropodidae). VI. Determination of the plesiomorphic karyotype: G-banding comparison of Thylogale with Petrogale persephone, P. xanthopus, and P. l. lateralis. Cytogenet. Cell Genet. 61: 29–33.[Medline]
EVGEN'EV, M. B., H. ZELENTSOVA, H. POLUECTOVA, G. T. LYOZIN, V. VELEIKODVORSKAJA et al., 2000 Mobile elements and chromosomal evolution in the virilis group of Drosophila. Proc. Natl. Acad. Sci. USA 97: 11337–11342.
FERRERI, G. C., M. MARZELLI, W. RENS and R. J. O'NEILL, 2004 A centromere-specific retroviral element associated with breaks of synteny in macropodine marsupials. Cytogenet. Genome Res. 107: 115–118.
FERRERI, G. C., D. M. LISCINSKY, J. A. MACK, M. D. ELDRIDGE and R. J. O'NEILL, 2005 Retention of latent centromeres in the mammalian genome. J. Hered. 96: 217–224.
FONTDEVILA, A., 1992 Genetic instability and rapid speciation: Are they coupled? Genetica 86: 247–258.[CrossRef]
FONTDEVILA, A., 2005 Hybrid genome evolution by transposition. Cytogenet. Genome Res. 110: 49–55.[CrossRef][Medline]
FUKAGAWA, T., M. NOGAMI, M. YOSHIKAWA, M. IKENO, T. OKAZAKI et al., 2004 Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat. Cell Biol. 6: 784–791.[CrossRef][Medline]
GREWAL, S. I., and S. JIA, 2007 Heterochromatin revisited. Nat. Rev. Genet. 8: 35–46.[CrossRef][Medline]
HAYMAN, D. L., 1990 Marsupial cytogenetics. Aust. J. Zool. 37: 331–349.[CrossRef]
HENIKOFF, S., and H. S. MALIK, 2002 Centromeres: selfish drivers. Nature 417: 227.[CrossRef][Medline]
HENIKOFF, S., K. AHMAD and H. S. MALIK, 2001 The centromere paradox: stable inheritance with rapidly evolving DNA. Science 293: 1098–1102.
HOUBEN, A., and I. SCHUBERT, 2003 DNA and proteins of plant centromeres. Curr. Opin. Plant Biol. 6: 554–560.[CrossRef][Medline]
KANELLOPOULOU, C., S. A. MULJO, A. L. KUNG, S. GANESAN, R. DRAPKIN et al., 2005 Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19: 489–501.
KEHRER-SAWATZKI, H., B. SCHREINER, S. TANZER, M. PLATZER, S. MULLER et al., 2002 Molecular characterization of the pericentric inversion that causes differences between chimpanzee chromosome 19 and human chromosome 17. Am. J. Hum. Genet. 71: 375–388.[CrossRef][Medline]
KING, M., 1993 Species Evolution: The Role of Chromosome Change. Cambridge University Press, Cambridge, UK.
LABRADOR, M., M. FARRE, F. UTZET and A. FONTDEVILA, 1999 Interspecific hybridization increases transposition rates of Osvaldo. Mol. Biol. Evol. 16: 931–937.[Abstract]
LIM, J. K., 1988 Intrachromosomal rearrangements mediated by hobo transposons in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 85: 9153–9157.
LIM, J. K., and M. J. SIMMONS, 1994 Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. BioEssays 16: 269–275.[CrossRef][Medline]
LIPPMAN, Z., and R. MARTIENSSEN, 2004 The role of RNA interference in heterochromatic silencing. Nature 431: 364–370.[CrossRef][Medline]
LOWRY, P. S., M. D. B. ELDRIDGE and P. G. JOHNSTON, 1995 Genetic analysis of a female macropodid hybrid (Macropus agilis x M. rufogriseus) and her backcross offspring. Aust. Mammal. 18: 79–82.
MALIK, H. S., and S. HENIKOFF, 2001 Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157: 1293–1298.
MALIK, H. S., and S. HENIKOFF, 2002 Conflict begets complexity: the evolution of centromeres. Curr. Opin. Genet. Dev. 12: 711–718.[CrossRef][Medline]
MARTIN, R., W. BUSCH, R. G. HERRMANN and G. WANNER, 1994 Efficient preparation of plant chromosomes for high-resolution scanning electron microscopy. Chromosome Res. 2: 411–415.[CrossRef][Medline]
MCCLINTOCK, B., 1929 Chromosome morphology in Zea Mays. Science 69: 629.
MCCLINTOCK, B., 1987 The Discovery and Characterization of Transposable Elements. Garland Publishing, New York.
MEISTER, G., and T. TUSCHL, 2004 Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343–349.[CrossRef][Medline]
MINIOU, P., M. JEANPIERRE, V. BLANQUET, V. SIBELLA, D. BONNEAU et al., 1994 Abnormal methylation pattern in constitutive and facultative (X inactive chromosome) heterochromatin of ICF patients. Hum. Mol. Genet. 3: 2093–2102.
O'NEILL, R. J., M. J. O'NEILL and J. A. MARSHALL GRAVES, 1998 Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 393: 68–72.[CrossRef][Medline]
O'NEILL, R. J., M. D. B. ELDRIDGE, R. TODER, M. A. FERGUSON-SMITH, P. C. O'BRIEN et al., 1999 Chromosome evolution in kangaroos (Marsupialia: Macropodidae): cross species chromosome painting between the tammar wallaby and rock wallaby spp. with the 2n = 22 ancestral macropodid karyotype. Genome 42: 525–530.[Medline]
O'NEILL, R. J., M. D. B. ELDRIDGE and J. A. M. GRAVES, 2001 Chromosome heterozygosity and de novo chromosome rearrangements in mammalian interspecies hybrids. Mamm. Genome 12: 256–259.[CrossRef][Medline]
O'NEILL, R. J., M. D. B. ELDRIDGE and C. J. METCALFE, 2004 Centromere dynamics and chromosome evolution in marsupials. J. Hered. 95: 375–381.
PAL-BHADRA, M., B. A. LEIBOVITCH, S. G. GANDHI, M. RAO, U. BHADRA et al., 2004 Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303: 669–672.
PARDO-MANUEL DE VILLENA, F., and C. SAPIENZA, 2001 Female meiosis drives karyotypic evolution in mammals. Genetics 159: 1179–1189.
RENS, W., P. C. M. O'BRIEN, F. YANG, J. A. M. GRAVES and M. A. FERGUSON-SMITH, 1999 Karyotype relationships between four distantly related marsupials revealed by reciprocal chromosome painting. Chromosome Res. 7: 461–474.[CrossRef][Medline]
ROFE, R. H., 1978 G-banded chromosomes and the evolution of the Macropodidae. Aust. Mammal. 2: 53–63.
RUIZ-HERRERA, A., J. CASTRESANA and T. ROBINSON, 2006 Is mammalian chromosomal evolution driven by regions of genome fragility? Genome Biol. 7: R115.[CrossRef][Medline]
SCHWARTZ, A., D. CHAN, L. BROWN, R. ALAGAPPAN, D. PETTAY et al., 1998 Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE-LINE recombination. Hum. Mol. Genet. 7: 1–11.
SHARMAN, G. B., 1961 The mitotic chromosomes of marsupials and their bearing on taxonomy and phylogeny. Aust. J. Zool. 9: 38–60.[CrossRef]
SUGIMOTO, K., H. YATA, Y. MURO and M. HIMENO, 1994 Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J. Biochem. 116: 877–881.
SUMNER, A., 1972 A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75: 304–306.[CrossRef][Medline]
SUMNER, A., 1998 The structure of the centromeric region of CHO chromosomes. Cell Biol. Int. 22(2): 127–130.[CrossRef][Medline]
SUMNER, A., 2003 Chromosomes: Organisation and Structure. Blackwell Science, Malden, MA.
TALBERT, P. B., T. D. BRYSON and S. HENIKOFF, 2004 Adaptive evolution of centromere proteins in plants and animals. J. Biol. 3: 18.[CrossRef][Medline]
UNGERER, M. C., S. C. STRAKOSH and Y. ZHEN, 2006 Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr. Biol. 16: R872–R873.[CrossRef][Medline]
VOLPE, T. A., C. KIDNER, I. M. HALL, G. TENG, S. I. S. GREWAL et al., 2002 Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297: 1833–1837.
VOLPE, T., V. SCHRAMKE, G. L. HAMILTON, S. A. WHITE, G. TENG et al., 2003 RNA interference is required for normal centromere function infission yeast. Chromosome Res. 11: 137–146.[CrossRef][Medline]
WANNER, G., and H. FORMANEK, 1995 Imaging of DNA in human and plant chromosomes by high-resolution scanning electron microscopy. Chromosome Res. 3: 368–374.[CrossRef][Medline]
WANNER, G., and H. FORMANEK, 2000 A new chromosome model. J. Struct. Biol. 132: 147–161.[CrossRef][Medline]
ZHANG, J., and T. PETERSON, 1999 Genome rearrangements by nonlinear transposons in maize. Genetics 153: 1403–1410.
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