High intrachromosomal similarity of retrotransposon long terminal repeats: evidence for homogenization by gene conversion on plant sex chromosomes?
ABSTRACT Retrotransposons are ubiquitous in the plant genomes and are responsible for their plasticity. Recently, we described a novel family of gypsy-like retrotransposons, named Retand, in the dioecious plant Silene latifolia possessing evolutionary young sex chromosomes of the mammalian type (XY). Here we have analyzed long terminal repeats (LTRs) of Retand that were amplified from laser microdissected X and Y sex chromosomes and autosomes of S. latifolia. A majority of X and Y-derived LTRs formed a few separate clades in phylogenetic analysis reflecting their high intrachromosomal similarity. Moreover, the LTRs localized on the Y chromosome were less divergent than the X chromosome-derived or autosomal LTRs. These data can be explained by a homogenization process, such as gene conversion, working more intensively on the Y chromosome.
- SourceAvailable from: ncbi.nlm.nih.gov[show abstract] [hide abstract]
ABSTRACT: Satellite DNA is an enigmatic component of genomic DNA with unclear function that has been regarded as "junk." Yet, persistence of these tandem highly repetitive sequences in heterochromatic regions of most eukaryotic chromosomes attests to their importance in the genome. We explored the Anopheles gambiae genome for the presence of satellite repeats and identified 12 novel satellite DNA families. Certain families were found in close juxtaposition within the genome. Six satellites, falling into two evolutionarily linked groups, were investigated in detail. Four of them were experimentally confirmed to be linked to the Y chromosome, whereas their relatives occupy centromeric regions of either the X chromosome or the autosomes. A complex evolutionary pattern was revealed among the AgY477-like satellites, suggesting their rapid turnover in the A. gambiae complex and, potentially, recombination between sex chromosomes. The substitution pattern suggested rolling circle replication as an array expansion mechanism in the Y-linked 53-bp satellite families. Despite residing in different portions of the genome, the 53-bp satellites share the same monomer lengths, apparently maintained by molecular drive or structural constraints. Potential functional centromeric DNA structures, consisting of twofold dyad symmetries flanked by a common sequence motif, have been identified in both satellite groups.Genetics 02/2005; 169(1):185-96. · 4.39 Impact Factor
Article: The degeneration of Y chromosomes.[show abstract] [hide abstract]
ABSTRACT: Y chromosomes are genetically degenerate, having lost most of the active genes that were present in their ancestors. The causes of this degeneration have attracted much attention from evolutionary theorists. Four major theories are reviewed here: Muller's ratchet, background selection, the Hill Robertson effect with weak selection, and the 'hitchhiking' of deleterious alleles by favourable mutations. All of these involve a reduction in effective population size as a result of selective events occurring in a non-recombining genome, and the consequent weakening of the efficacy of selection. We review the consequences of these processes for patterns of molecular evolution and variation at loci on Y chromosomes, and discuss the results of empirical studies of these patterns for some evolving Y-chromosome and neo-Y-chromosome systems. These results suggest that the effective population sizes of evolving Y or neo-Y chromosomes are severely reduced, as expected if some or all of the hypothesized processes leading to degeneration are operative. It is, however, currently unclear which of the various processes is most important; some directions for future work to help to resolve this question are discussed.Philosophical Transactions of The Royal Society B Biological Sciences 12/2000; 355(1403):1563-72. · 6.23 Impact Factor
- [show abstract] [hide abstract]
ABSTRACT: The male-specific region of the Y chromosome, the MSY, differentiates the sexes and comprises 95% of the chromosome's length. Here, we report that the MSY is a mosaic of heterochromatic sequences and three classes of euchromatic sequences: X-transposed, X-degenerate and ampliconic. These classes contain all 156 known transcription units, which include 78 protein-coding genes that collectively encode 27 distinct proteins. The X-transposed sequences exhibit 99% identity to the X chromosome. The X-degenerate sequences are remnants of ancient autosomes from which the modern X and Y chromosomes evolved. The ampliconic class includes large regions (about 30% of the MSY euchromatin) where sequence pairs show greater than 99.9% identity, which is maintained by frequent gene conversion (non-reciprocal transfer). The most prominent features here are eight massive palindromes, at least six of which contain testis genes.Nature 07/2003; 423(6942):825-37. · 38.60 Impact Factor
High intrachromosomal similarity of retrotransposon long terminal
repeats: Evidence for homogenization by gene conversion on
plant sex chromosomes?
Eduard Kejnovskya,⁎, Roman Hobzaa, Zdenek Kubata, Alex Widmerb,
Gabriel A.B. Maraisc, Boris Vyskota
aLaboratory of Plant Developmental Genetics, Institute of Biophysics, Academy of Sciences of the Czech Republic, Kralovopolska 135,
CZ-612 65 Brno, Czech Republic
bInstitute of Integrative Biology, Plant Ecological Genetics, Universitaetstrasse 16, 8092 Zurich, Switzerland
cLaboratoire de Biométrie et Biologie Evolutive (UMR 5558); CNRS; University Lyon 1, Bat. Gregor Mendel, 16 rue Raphaël Dubois,
69622, Villeurbanne Cedex, France
Received 14 June 2006; received in revised form 3 October 2006; accepted 3 October 2006
Available online 24 October 2006
Retrotransposons are ubiquitous in the plant genomes and are responsible for their plasticity. Recently, we described a novel family of gypsy-like
retrotransposons, named Retand, in the dioecious plant Silene latifolia possessing evolutionary young sex chromosomes of the mammalian type
(XY). Here we have analyzed long terminal repeats (LTRs) of Retand that were amplified from laser microdissected X and Y sex chromosomes and
autosomes of S. latifolia. A majority of X and Y-derived LTRs formed a few separate clades in phylogenetic analysis reflecting their high
intrachromosomal similarity.Moreover, the LTRs localized on the Y chromosome were less divergent than the X chromosome-derived or autosomal
LTRs. These data can be explained by a homogenization process, such as gene conversion, working more intensively on the Y chromosome.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Repetitive DNA; Sex chromosomes; Dioecious plant; Microdissected chromosomes; Genome evolution
evolve in a concerted fashion which results in their homogeni-
zation. One of the mechanisms responsible for concerted
evolution is gene conversion (Liao, 2003). Gene conversion is
to replacement of one allele by another. It consists in copying of
one stretch of DNA into another. Gene conversion is likely to be
involved in homogenization of ribosomal DNA arrays (Schlot-
terer and Tautz, 1994) as well as satellites (Elder and Turner,
1995; Schueler et al., 2001). The rate of homogenization of such
repetitive sequences is higher along chromosomal lineages than
between different chromosomes (Warburton and Willard, 1995).
centromeres, which is primarily homogenized in a chromosome-
specific manner (Schueler et al., 2001).
Homogenization of transposable elements, which represent
interspersed repeats, is less understood. Most families of mobile
elementsare classifiedintoseveral families; someare ancient and
others more recent. Elements that are still active in retroposition
have a higher degree of sequence similarity, which reflects recent
conversion also in transposable elements. The influence of gene
conversion was presented in the MITE elements of A. thaliana
(Le et al., 2000), human Alu elements (Roy et al., 2000) and S2
elements of D. melanogaster (Maside et al., 2003). Kass et al.
(1995) reported a gene conversion event in which one of the
oldest Alu family members was converted to one of the youngest
Alu subfamilies, Yb8. Hood et al. (2005) electrophoretically
Gene 390 (2007) 92–97
Abbreviations: FISH, fluorescence in situ hybridization; PCR, polymerase
chainreaction;bp, basepair(s); dNTP,deoxyribonucleosidetriphosphate;DAPI,
⁎Corresponding author. Tel.: +420 541517203; fax: +420 541240500.
E-mail address: email@example.com (E. Kejnovsky).
URL: http://www.ibp.cz/labs/PDG/ (E. Kejnovsky).
0378-1119/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
separated chromosomes of Microbotryum violaceum and studied
the structure of copia and Helitron transposable elements. They
showed a statistically significant similarity among copies
originated from the same chromosome which is consistent with
the gene conversion hypothesis (Hood et al., 2005).
In sexually reproducing organisms the homogenization
processes are significantly accelerated by meiotic recombina-
tion. Repetitive satellite sequences are more homogenous in
insect species that undergo sexual reproduction than those in
asexual species (Mantovani, 1998), which indicates that meiotic
recombination plays a major role in sequence homogenization.
The gene conversion among copies of satellite DNA located on
the sex chromosomes was demonstrated for the first time in
Anopheles gambiae (Krzywinski et al., 2005). Phylogenetic
analysis revealed that satellite DNA monomers originating from
the Yand X chromosomes formed separate clades. Two possible
mechanisms were proposed to explain the Y-linked array
expansion in non-recombining Y chromosome in A. gambiae.
They included unequal sister chromatid exchange (Smith, 1976)
the genome (Okumura et al., 1987).
Recently, we described a new family of gypsy-like retro-
transposons, named Retand (Kejnovsky et al., 2006). These
retrotransposons are transcriptionally active and are highly
abundant in Silene latifolia, the dioecious plant with hetero-
morphic sex chromosomes. Here we show that long terminal
repeats (LTRs) of the Retand retrotransposons isolated from
laser microdissected X and Y chromosomes of S. latifolia are
more similar to copies in the respective chromosome than to
than the X-linked or autosomal LTRs. This phenomenon can be
explained by the mechanism of gene conversion.
2. Materials and methods
2.1. Microdissection of chromosomes, PCR amplification of
LTRs and DNA sequence analysis
Mitotic X and Y sex chromosomes and autosomes were
microdissected and collected as described by Hobza et al. (2004).
Ten individual Yand X chromosomes, or 110 autosomes (10 of
each),wereusedfor each PCRreaction. To amplifyRetandLTRs
we used PCR with the primers: LTR-F1 (5′-TTCCGGGTGTA-
ATTCCAGAG-3′) and LTR-R1 (5′-CATATTCTGCACCCGCT-
GAC-3′), that produced dominant PCR product with a length of
about 600 bp (Kejnovsky et al., 2006). The reactions were
performed in a volume of 50 μl, and the final concentration of
containing 1.5 mM MgCl2, and 0.6 U of Taq polymerase
94 °C, 1 min at 55 °C, and 1 min at 72 °C, with a final extension
for 7 min. The PTC-200 thermal cycler (MJ Research) was used.
PCR products were purified using the Qiagen PCR purification
kit, cloned using the pGEM-T Easy cloning system (Invitrogen),
and sequenced using the BigDye Terminator sequencing kit
All sequences were read twice and the clone sequences were
assembled with Staden Package software (Staden, 1996). The
paper are: DQ683758–DQ683969 and DQ922567–DQ922629.
Multiple sequence alignments were performed with ClustalW
(Thompson-Stewart et al., 1994) and phylogenetic trees were
et al., 2005) using the following parameters: HKY model,
estimated frequency of invariants, estimated transition over
transversion ratio, gamma-distribution: 4 site categories, alpha
2.2. Fluorescence in situ hybridization
Inorder tosynchronize germinatingseeds ofS.latifolia (seeds
Czech Republic), the DNA polymerase inhibitor aphidicolin was
Slides were treated as described in Lengerova et al. (2004)
with slight modifications. Slide denaturation was performed in
7:3 (v/v) formamide:2× SSC for 2 min at 72 °C. Slides were
immediately dehydrated through 50%, 70%, and 100% ethanol
(−20 °C), and air dried. The probe was denatured at 70 °C for
10 min, and 100 ng of the denatured probe was added and
hybridized for 18 h at 37 °C. Slides were analyzed using an
Olympus Provis microscope, and image analysis was performed
using ISIS software (Metasystems). DNA was labeled with
Fluorolink Cy3-dUTP (Amersham Pharmacia Biotech) in
combination with the nick translation mix (Roche).
3. Results and discussion
3.1. Amplification of Retand long terminal repeats (LTRs) on
microdissected chromosomes and their phylogenetic analysis
We amplified LTRs from microdissected Y chromosomes, X
chromosomes and autosomes by primers designed according to
the Retand-1 element (Kejnovsky et al., 2006). Amplification
resulted in a single PCR product which was cloned to construct
three separate libraries. We sequenced 73 Y chromosome-
derived LTRs, 86 X chromosome-derived LTRs, and 116 LTRs
of autosomal origin.
The sequences of all LTRs were aligned with ClustalW and
the phylogenetic tree was constructed using PHYML (Guindon
and Gascuel, 2003; Guindon et al., 2005). The phylogenetic
analysis showed that LTRs from the Y chromosome as well as
those from the X chromosome form separate groups divergent
from the LTRs amplified on the autosomes. The Y-linked LTRs
had only several larger groups (Fig. 1, the larger Y group
comprises ∼50 LTRs). Moreover, the Y-linked LTRs had a very
high within group similarity that was not regularly found for the
X-linked and only rare for the autosomal LTRs. Table 1 reports
the redundancy among LTRs, the number of polymorphic sites
andthemean pair-wisedifferences between LTRsequences,and
LTR nucleotide diversity. Genetic diversity was highest in the
sample of LTR sequences from the autosomes, and lowest in
LTRs from the Y chromosome, and pair-wise differences
93E. Kejnovsky et al. / Gene 390 (2007) 92–97
between LTR sequences were lowest for Y-derived LTRs, which
reflects the strong tendency for these sequences to form groups
in the phylogenetic analysis.
An interesting phenomenon is the presence of several Yor X
chromosome-derived LTR sequences among autosome-derived
LTR sequences (see the arrows in Fig. 1). We suggest that these
LTR sequences of the autosomal type located on the X or Y
chromosomes could be a result of their recent transfer from
autosomes to the sex chromosomes (more frequently than vice
versa). Similarly, the SlAP3 MADS box gene has been
Fig. 1. Phylogenetic analysis of LTRs amplified on the X and Y chromosomes and autosomes of S. latifolia. LTR sequences were aligned with ClustalW (Thompson-
Stewart et al., 1994), the phylogenetic tree was constructed using PHYML software (Guindon and Gascuel, 2003; Guindon et al., 2005). The tree is unrooted. Several
origin — X chromosomes (blue squares), Y chromosomes (red triangles) or autosomes (black circles). Red or blue arrows indicate Yor X chromosome-derived LTRs of
for the X- and Y-clades (N2 sequences) are indicated.
94 E. Kejnovsky et al. / Gene 390 (2007) 92–97
duplicatively transferred from an autosome onto the Y chromo-
some in S. latifolia (Matsunaga et al., 2003). Gene traffic on and
off a sex chromosome, mostly by retrotransposition, has been
already reported for the human X chromosome (Emerson et al.,
2004; Khil et al., 2005).
3.2. Chromosomal localization of Retand LTRs by FISH
In order to know the relative representation of LTRs of Re-
tand elements on different chromosomes we studied chromo-
somal localization of the Retand elements by fluorescence in
situ hybridization (FISH). When the LTR was used as a probe
for FISH on metaphase chromosomes of S. latifolia, strong
subtelomeric signals were present on all chromosomes (Fig. 2).
The only one exception was the Y chromosome where signal
was absent on the p arm (Lengerova et al., 2003, 2004). From
this we can derive that the Y chromosome harbors only about
half the number of Retand LTRs present on the other
chromosomes. In addition to subtelomeric signals, dispersed
signals covering also other parts of chromosomes were
observed. In most chromosomes both subtelomeres of the
same chromosome carried a signal of similar intensity, only a
few had rather asymmetric signal intensity.
3.3. Gene conversion, preferential intrachromosomal retro-
transposition or methodological caveat?
A higher intrachromosomal similarity seen in Fig. 1 and
a low level of nucleotide polymorphism among copies pre-
sented in Table 1 of the Y- or X-linked LTRs could be explained
by homogenization of the elements on the sex chromosomes by
processes such as gene conversion. This process is, according
to our data, more intensive on the Y chromosome, where the
homogeneity of LTRs is much higher. Alternatively, the low
variability of Y-derived LTR sequences could be a consequence
of loss of diversity within local populations due to genetic
drift. Filatov (2000) and Ironside and Filatov (2005) described
the lower variability in Y-linked genes to their X-linked ho-
mologues in S. latifolia and discussed the role of selective
sweep, background selection and Muller's ratchet. These
processes are predicted to severely affect the evolution of the
non-recombining Y chromosome and could also account here
described phenomena. However, all studies comparing differ-
ences between rates of mutation and/or fixation among sex-
linked vs. autosomal genes were based on comparison of ortho-
logous or allelic sequences. Here we are comparing paralogous
sequences — all the sequences belong to the Retand family of
the same individual.
Our results are interesting in the light of the recent
discoveries in mammals where gene conversion was proposed
to explain a higher similarity than expected between some X–Y
gene copies (Pecon Slattery et al., 2000; Marais and Galtier,
2003; Skaletsky et al., 2003). Gene conversion stands also
behind the high identity of large palindromes on the human Y
chromosome (Skaletsky et al., 2003; Rozen et al., 2003). This
process seems to protect essential genes from degeneration that
is an inevitable consequence of lack of meiotic recombination
(Charlesworth, 2003; Charlesworth and Charlesworth, 2000).
The lack of a meiotic pairing partner probably leaves the Y
chromosome free to fold back onto itself (Hurtles and Jobling,
2003). Based on our data, we suggest that this mechanism of
intrachromosomal gene conversion on the Y chromosome is
even more efficient that gene conversion working on the other
chromosomes undergoing normal meiotic pairing. We can
speculate that homogenization of Retand LTRs could be
somehow connected with its occurrence at subtelomeres
where tandem repeats, which could be a good target for gene
conversion, are located in S. latifolia (Buzek et al., 1997).
Chromosome-specific pattern of Retand LTRs can be
alternatively explained by preferential intrachromosomal retro-
transposition, i.e., new copies of retrotransposons can integrate
into the chromosome-of-origin resulting in the observed
similarities within chromosomes. This is, however, unlikely
because transcripts of retrotransposons leave the nucleus for
reverse transcription prior to integration. Some targeting of
Molecular diversity of LTR sequences derived from S. latifolia chromosomes
LTRs derived from # LTRs sequenced# redundant LTRs (%)a
# polymorphic sites Mean pair-wise differences (±sd)Nucleotide diversity (±sd)
aRedundant LTR sequences determined after removal of all gaps.
Fig. 2. Metaphase chromosomes of S. latifolia were hybridized with LTR.
Chromosomes werecounterstainedwithDAPI (here inred); probeswerelabeled
with Cy3-conjugated nucleotides (here signals are in green). The X and Y
chromosomes are indicated, bar=10 μm.
95E. Kejnovsky et al. / Gene 390 (2007) 92–97
elements was demonstrated for particular chromosomal regions,
such as telomeric or subtelomeric repeats as well as rDNA loci
(Anzai et al., 2001; Xie et al., 2001; Zhu et al., 2003). However,
the chromosomal specificity of integration necessary to explain
our results is not known. Higher homogeneity of Y-linked LTRs
could bealso explainedbymany more recentretrotranspositions
of active Retand elements directed onto the Y chromosome in
contrast to older X chromosomal or autosomal Retand
insertions. Thus, recently inserted elements should be more
homogenous than more divergent older elements.
The three different libraries of the LTRs that we have made
(the X, Y, autosomes) do not have the same complexity (i.e.,
number of non-redundant clones). Assuming a similar number
of Retand copies at each subtelomere, we expect the autosomal
library to have a greater complexity because it contains LTRs
from 11 different chromosomes. The Y library should have the
lowest complexity because it contains LTRs from the only Y
chromosome for which the Retand copies are located only at the
asymmetric subtelomere. Finally, the X library should have a
slightly higher complexity than the Y because it has Retand at
both subtelomeric regions. With 73 sequenced clones from the
Y library, 86 sequenced clones from the X library, and 116 from
the autosomal one, we have differences in sampling effort
between libraries. The chance to sequence several times the
same copy is quite strong in the case of the Y chromosome, a bit
lower for the X, and it is very low for the autosomes. Repeated
sequencing of the same copies could explain the existence of
groups of homogeneous sequences for the X and Y chromo-
somes (Fig. 1). However, the sequences belonging to the Yor X
groups are not identical as expected in the case of repeated
sequencing of the same copies, which tend to suggest that the
methodological caveat mentioned can not explain our data. In
addition, we designed the test for ascertainment bias. We re-
sampled X and Y sequences to get the same number of sampled
sequences per chromosome between sex chromosomes and
autosomes, we consider that we had 116 Retand sequences from
11 autosomes, which gives ~10 Retand sequences per
autosome, so we re-sampled 10 of 86 Retand X sequences
and 10 of 73 Retand Y sequences. In all 5 re-samplings the
phylogenetic trees were similar to the original tree containing all
sequences, i.e. LTRs from the Y chromosome as well as those
from the X chromosome formed separate groups divergent from
the LTRs amplified on the autosomes (data not shown).
Our results support the idea of a high intensity of
homogenization on the Y chromosome in S. latifolia. However,
in another dioecious plant Rumex acetosa possessing two Y
chromosomes (XY1Y2), the variability of Y-associated satellite
DNAs was shown to be higher than variability of autosomal
satellites (Navajas-Perez et al., 2005). This result supports a
homogenization of the two non-recombining Y chromosomes.
Since the Y chromosomes of R. acetosa are evolutionary older
than the Y chromosome of S. latifolia, the differences in the
intensity of homogenization could reflect the different stages of
the Y chromosome evolution. If the repetitive elements are more
diverged,ascould betruefor the older Y chromosome, then gene
conversion is likely not to work on them.
In summary, we conclude that:
similarity of LTRs of Retand retrotransposons amplified
from microdissected sex chromosomes of S. latifolia,
(2) Intrachromosomal similarity of Retand LTRs originating
from the Y chromosome is higher than in the case of X
(3) We suggest that gene conversion homogenizing LTRs is a
more probable explanation of their higher intrachromo-
somal similarity than preferential intrachromosomal
This research was supported by the Czech Science Founda-
tion (grant nos. 204/05/2097 to E.K., 204/05/H505 and 521/06/
0056 to B.V.), and the Swiss Science Foundation (grant no.
Anzai, T., Takahashi, H., Fujiwara, H., 2001. Elimination of active Tad elements
during the sexual phase of the Neurospora crassa life cycle. Fungal Genet.
Biol. 33, 49–57.
Buzek, J., et al., 1997. Isolation and charecterization of X chromosome-derived
DNA sequences from a dioecious plant Melandrium album. Chromosome
Res. 5, 57–65.
Charlesworth, B., 2003. The organization and evolution of the human Y chro-
mosome. Genome Biol. 4 (Art. No. 226).
Charlesworth, B.,Charlesworth, D.,2000.The degenerationof Y chromosomes.
Philos. Trans. R. Soc. Lond., B Biol. Sci. 355, 1563–1572.
Elder Jr., J.F., Turner, B.J., 1995. Concerted evolution of repetitive DNA
sequences in eukaryotes. Q. Rev. Biol. 70, 297–320.
Emerson, J.J., Kaessmann, H., Betran, E., Long, M., 2004. Extensive gene
traffic on the mammalian X chromosome. Science 303, 537–540.
Filatov, D.A., 2000. Low variability in a Y-linked plant gene and its implications
for Y-chromosome evolution. Nature 404, 388–390.
Guindon, S., Gascuel, O., 2003. A simple, fast, and accurate algorithm to
server for fast maximum likelihood-based phylogenetic inference. Nucleic
Acids Res. 33, 557–559.
Hobza, R., Lengerova, M., Cernohorska, H., Rubes, J., Vyskot, B., 2004. FAST-
FISH with laser beam microdissected DOP-PCR probe distinguishes the sex
chromosomes of Silene latifolia. Chromosome Res. 12, 245–250.
Hood, M.E., Katawczik, M., Giraud, T., 2005. Repeat-induced point mutation and
the population structure of transposable elements in Microbotryum violaceum.
Genetics 170, 1081–1089.
Hurtles, M.E., Jobling, M.A., 2003. A singular chromosome. Nat. Genet. 34,
Ironside, J.E., Filatov, D.A., 2005. Extreme population structure and high
interspecific divergence of theSilene Y chromosome. Genetics 171, 705–713.
Kass, D.H., Batzer, M.A., Deininger, P.L., 1995. Gene conversion as a
secondary mechanism in SINE evolution. Mol. Cell. Biol. 15, 19–25.
Kejnovsky, E., Kubat, Z., Macas, J., Hobza, R., Vyskot, B., 2006. RETAND: a
novel family of gypsy-like retrotransposon harboring an amplified tandem
repeat. Mol. Gen. Genom. 276, 254–263.
Khil, P.P., Oliver, B., Camerini-Otero, R.D., 2005. X for intersection:
retrotransposition both on and off the X chromosome is more frequent.
Trends Genet. 21, 3–7.
96E. Kejnovsky et al. / Gene 390 (2007) 92–97
Krzywinski, J., Sangare, D., Besansky, N.J., 2005. Satellite DNA from the Y
chromosome of the malaria vector Anopheles gambiae. Genetics 169,
Le, Q.H., Wright, S., Yu, Z., Bureau, T., 2000. Transposon diversity in Arabi-
dopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 97, 7376–7381.
of Silene latifolia revisited and revised. Genetics 165, 935–938.
Lengerova, M., Kejnovsky, E., Hobza, R., Macas, J., Grant, S.R., Vyskot, B.,
2004. Multicolour FISH mapping of the dioecious model plant, Silene
latifolia. Theor. Appl. Genet. 108, 1193–1199.
Liao, D., 2003. Concerted evolution. In: Encyclopedia of the Human Genome.
Macmillian Publishers Ltd, Nature Publishing Group, London, pp. 1–6.
Mantovani, B., 1998. Satellite sequence turnover in parthenogenetic systems:
the apomictic triploid hybrid Bacillus lynceorum (Insecta, Phasmatodea).
Mol. Biol. Evol. 15, 1288–1297.
Marais, G., Galtier, N., 2003. Sex chromosomes: how X–Y recombination stops.
Curr. Biol. 13, R641–R643.
Maside, X., Bartolome, C., Charlesworth, B., 2003. Inferences on the
evolutionary histrory of the S-element family of Drosophila melanogaster.
Mol. Biol. Evol. 20, 1183–1187.
Matsunaga, S., Isono, E., Kejnovsky, E., Vyskot, B., Kawano, S., Charlesworth,
D., 2003. Duplicative transfer of MADS box gene to a plant Y chromosome.
Mol. Biol. Evol. 20, 1062–1069.
Navajas-Perez, R., et al., 2005. Reduced rates of sequence evolution of Y-linked
satellite DNA in Rumex (Polygonaceae). J. Mol. Evol. 60, 391–399.
Okumura, K., Kiyama, R., Oishi, M., 1987. Sequence analysis of extrachro-
mosomal Sau3A and related family DNA: analysis of recombination in the
excision event. Nucleic Acids Res. 15, 7477–7489.
Pecon Slattery, J., Sanner-Wachter, L., O'Brien, S.J., 2000. Novel gene conver-
sion between X–Y homologues located in the nonrecombining region of the
Y chromosome in Felidae (Mammalia). Proc. Natl. Acad. Sci. U. S. A. 97,
Rozen, S., et al., 2003. Abundant gene conversion between arms of palindromes
in human and ape Y chromosome. Nature 423, 873–876.
Roy, A.M., et al., 2000. Potential gene conversion and source genes for recently
integrated Alu elements. Genome Res. 10, 1485–1495.
Schlotterer, C., Tautz, D., 1994. Chromosomal homogeneity of Drosophila
ribosomal DNA arrays suggests intrachromosomal exchanges drive
concerted evolution. Curr. Biol. 4, 777–783.
Schueler, M.G., Higgins, A.W., Rudd, M.K., Gustashaw, K., Willard, H.F.,
2001. Genomic and genetic definition of a functional human centromere.
Science 294, 109–115.
Skaletsky, H., et al., 2003. The male-specific region of the human Y
chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837.
Smith, G.P., 1976. Evolution of repeated DNA sequences by unequal crossover.
Science 191, 528–535.
Staden, R., 1996. The Staden sequence analysis package. Mol. Biotechnol. 5,
Thompson-Stewart, D., Karpen, G.H., Spradling, A.C., 1994. A transposable
element can drive the concerted evolution of tandemly repetitious DNA.
Proc. Natl. Acad. Sci. U. S. A. 91, 9042–9046.
Warburton, P.E., Willard, H.F., 1995. Interhomolog sequence variation of alpha
satellite DNA from human chromosome 17: evidence for concerted
evolution along haplotypic lineages. J. Mol. Evol. 41, 1006–1015.
Xie, W.W., Gai, X., Zhu, Y., Zappulla, D.C., Sternglanz, R., Voytas, D., 2001.
Targeting of the yeast Ty5 retrotransposon to silent chromatin is mediated by
interactions between integrase and Sir4p. Mol. Cell. Biol. 21, 6606–6614.
Zhu, Y., Dai, J., Fuerst, P.G., Voytas, D.F., 2003. Controlling integration
specificity of a yeast retrotransposon. Proc. Natl. Acad. Sci. U. S. A. 100,
97 E. Kejnovsky et al. / Gene 390 (2007) 92–97