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Junk DNA promotes sex chromosome evolution

DOI:10.1038/hdy.2009.36
Authors:
Sachihiro Matsunaga at Tokyo University of Science
Sachihiro Matsunaga
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NEWS AND COMMENTARY
Sex chromosome
...............................................................
Junk DNA promotes sex
chromosome evolution
S Matsunaga
...........................................................
Heredity (2009) 102, 525–526; doi:10.1038/hdy.2009.36; published online 1 April 2009
Sex chromosomes evolved from a
pair of autosomes, independently,
in various phyla at different times.
After the appearance of the gene in-
volved in heterogametic male (XY)
determination on the ancient Y chromo-
some, extensive recombination sup-
pression evolved between ancient sex
chromosomes. Theoretically, the ancient
Y chromosome then suffered from
a rapid accumulation of deleterious
mutations and loss-of-function genes
(Charlesworth et al., 2005). As a result,
‘gene deserts’ or gene-poor heterochro-
matin regions became distributed over
the Y chromosome. As it is the fate of Y
chromosomes to become inert and
therefore, disappear from the male
genome at some point in the future,
they must be pitied.
Junk DNA, including transposable
elements (TEs) and non-coding repeti-
tive sequences, has been widely noted
as an evolutionary force for producing
novel gene function, and inducing
chromosome rearrangements and gen-
ome diversification (Biemont and Vieira,
2006). Accumulation of these junk DNA
sequences also contributes to the pro-
duction of the gene deserts found in the
Y chromosome. Kejnovsky
`et al. (2008)
have recently discussed the potential
for junk DNA accumulation to start at
an early stage in the evolution of sex
chromosomes. Both past cytogenetic
analyses and recent genome projects
have revealed that many animal Y
chromosomes have more abundant het-
erochromatin derived from repetitive
sequences compared with X chromo-
somes and autosomes. Accumulation of
repetitive sequences induces abnormal
recombination and chromosome breaks.
Thus, junk DNA accumulation may
well be a factor in the generation of
differences in morphology and size
observed between X and Y chromo-
somes; for example, in both the fruit fly
Drosophila melanogaster and in humans,
the Y chromosome is drastically smaller
than the X chromosome. The hetero-
chromatic regions distributed over more
than half of the human Y chromosome
originated B300 million years ago
(m.y.a.), and the D. melanogaster Y
chromosome, which was formed at least
60 m.y.a., has become almost entirely
heterochromatic (Adams et al., 2000;
Skaletsky et al., 2003). The Neo-Y chro-
mosome of Drosophila miranda formed
by a Y-autosome fusion only 1.2Bm.y.a.
still harbors many functional genes.
Even in this much younger Y chromo-
some, there is a more than 20-fold
greater accumulation of repetitive se-
quences, mainly transposable elements,
compared with that in the X chromo-
some (Bachtrog et al., 2008). These
findings in animal species show that
the accumulation of junk DNA is an
important step in promoting the mor-
phogenesis of sex chromosomes.
Junk DNA accumulation on Y chro-
mosomes has been believed to be a
symptom of Y-chromosome degenera-
tion. Insertion of repetitive sequences
into coding genes and regulatory
regions induces alteration in the genes’
functions and results in gene loss.
However, there is no correlation be-
tween the insertion of the transposable
element and gene dysfunction on the Y
chromosome of D. miranda (Bachtrog
et al., 2008). Moreover, the rate of gene
gain on the Drosophila Y chromosome—
using the sequences of 12 species—is
more than 10 times the rate of gene loss,
in contrast with the mammalian Y
chromosome (Koerich et al., 2008). The
contradiction between gene acquisition
and accumulation of highly repetitive
sequences on the Drosophila Y chromo-
somes, indicates that junk DNA accu-
mulation is not always directly
connected with Y chromosome degen-
eration.
To answer the question of how sex
chromosomes are formed and evolve,
we should survey more sex chromo-
somes in different taxa, including
plants. The majority of plant species
does not have sex chromosomes,
making dioecious species (with male
and female functions on separate
plants) a minority, in contrast to
animals. However, plant sex chromo-
somes have been found from moss to
flowering plants, including familiar
crop species, such as asparagus,
hop, kiwi fruit, papaya and spinach
(Matsunaga and Kawano, 2001). The
ancient Y chromosome in the liverwort
Marchantia polymorpha is small and
largely heterochromatic (Yamato et al.,
2007), whereas most Y chromosomes in
flowering plants are the largest chromo-
somes in male genomes and many plant
sex chromosomes are morphologically
indistinguishable (Matsunaga, 2006;
Jamilena et al., 2008). Why do sex
chromosomes in flowering plants seem
to retain their primitive characteristics
similar to a pair of autosomes? One
possible answer is that the plant sex
chromosomes are evolutionarily very
young. Thus, the study of sex chromo-
somes in flowering plants may allow us
to catch a glimpse of the early stages of
the genetic separation between males
and females. For example, it will give us
the opportunity to study the problem
of whether junk DNA accumulation
occurs before or after gene degeneration
on Y chromosomes (Marais et al.,
2008).
Kejnovsky
`et al. (2008) reported
that the accumulation of repetitive
sequences was generally found in the
evolutionarily young plant Y chromo-
somes. The papaya Y chromosome is
the youngest in plants, having diverged
from the X chromosome only 2–3 m.y.a.
(Liu et al., 2004). Even in such young Y
chromosomes, the accumulation of re-
petitive sequences and heterochromati-
nization can be detected.
The White Campion, Silene latifolia,is
a flowering plant whose sex chromo-
somes were first discovered in 1923; the
Y and X chromosomes are the largest
and second-largest chromosomes of the
male S. latifolia (Figure 1), respectively.
The Y chromosome evolved in the Silene
genus 10–20 m.y.a. through chromoso-
mal inversion (Armstrong and Filatov,
2008). There is a large accumulation of
microsatellites derived from repetitive
sequences on the young and large Y
chromosomes, whereas transposable
elements were found to be uniformly
distributed along both sex chromo-
somes. Interestingly, chloroplast DNA
also preferentially inserts into the Y
chromosome. These studies strongly
suggest that the accumulation of repeti-
tive sequences is a crucial and common
event in the early process of formation
of plant and animal sex chromosomes,
although the level of accumulation and
types of repetitive sequences are varied.
However, there is another possible
plant-specific function of repetitive
sequences during sex chromosome
evolution because, unlike animals,
plant genomes have increased through
Heredity (2009) 102,525–526
&
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repetition by whole genome duplication
with amplification of repetitive se-
quences. Such junk DNA accumulation
could contribute to increasing the size of
plant Y chromosomes and keep the
largest amount of DNA in the male
genome. A more detailed investigation
of young sex chromosomes in flowering
plants promises new insights into fun-
damental issues of the birth and evolu-
tion of sex chromosomes.
Associate Professor S Matsunaga is at the Labora-
tory of Dynamic Cell Biology, Department of
Biotechnology, Osaka University, Graduate School
of Engineering, 2-1 Yamadaoka, Suita, Osaka,
565-8652, Japan.
e-mail: sachi@bio.eng.osaka-u.ac.jp
Adams MD, Celniker SE, Holt RA, Evans CA,
Gocayne JD, Amanatides PG et al. (2000). The
genome sequence of Drosophila melanogaster.
Science 287: 2185–2195.
Armstrong SJ, Filatov DA (2008). A cytogenetic
view of sex chromosome evolution in plants.
Cytogenet Genome Res 120: 241–246.
Bachtrog D, Hom E, Wong KM, Maside X, de Jong
P (2008). Genomic degradation of a young Y
chromosome in Drosophila miranda.Genome Biol
9: R30.
Biemont C, Vieira C (2006). Junk DNA as an
evolutionary force. Nature 443: 521–524.
Charlesworth D, Charlesworth B, Marais G (2005).
Steps in the evolution of heteromorphic sex
chromosomes. Heredity 95: 118–128.
Jamilena M, Mariotti B, Manzano S (2008). Plant
sex chromosomes: molecular structure and
function. Cytogenet Genome Res 120: 255–264.
Kejnovsky
`E, Hobza R, Cerma
´k T, Kuba
´tZ,
Vyskot B (2008). The role of repetitive DNA
in structure and evolution of sex chromosomes
in plants. Heredity 102: 533–541.
Koerich LB, Wang X, Clark AG, Carvalho AB
(2008). Low conservation of gene content in
the Drosophila Y chromosome. Nature 456:
949–951.
Marais GAB, Nicolas M, Bergero R, Chambrier P,
Kejnovsky E, Moneger F et al. (2008). Evidence
for degeneration of the Y chromosome
in the dioecious plant Silene latifolia.Curr Biol
18: 1–5.
Matsunaga S, Kawano S (2001). Sex determination
by sex chromosomes in dioecious plants. Plant
Biol 3: 481–488.
Matsunaga S (2006). Sex chromosome-linked
genes in plants. Genes Genet Syst 81: 219–226.
Liu Z, Moore PH, Ma H, Ackerman CM, Ragiba
M, Yu Q et al. (2004). A primitive Y chromo-
some in papaya marks incipient sex chromo-
some evolution. Nature 427: 348–352.
Skaletsky H, Kuroda-Kawaguchi T, Minx PJ,
Cordum HS, Hillier L, Brown LG et al. (2003).
The male-specific region of the human Y
chromosome is a mosaic of discrete sequence
classes. Nature 423: 825–837.
Yamato KT, Ishizaki K, Fujisawa M, Okada S,
Nakayama S, Fujishita M et al. (2007). Gene
organization of the liverwort Y chromosome
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6472–6477.
Editor’s suggested reading
Greeff JM, Jansen van Vuuren GJ, Kryger P,
Moore JC (2009). Outbreeding and possibly
inbreeding depression in a pollinating fig
wasp with a mixed mating system. Heredity
102: 349–356.
de Boer JG, Ode PJ, Vet LEM, Whitfield JB,
Heimpel GE (2007). Diploid males sire
triploid daughters and sons in the parasitoid
wasp Cotesia vestalis.Heredity 99: 288–294.
Wilfert L, Gadau J, Schmid-Hempel P (2007).
Variation in genomic recombination rates
among animal taxa and the case of social
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Figure 1 The large X and Y chromosomes in Silene latifolia. Yellow signals represent
subtelomeric repetitive sequences. The right upper and lower flowers of S. latifolia are male
and female with XY and XX chromosomes, respectively. The color reproduction of this figure
is available on the html full text version of the manuscript.
News and Commentary
526
Heredity
... The repeatome is involved in the processes of sex chromosome differentiation [11,[40][41][42][43]. Both plants and animals have accumulated TEs and satDNAs in the nonrecombining regions of Y and W chromosomes [11,40,[42][43][44][45][46]. ...
... The repeatome is involved in the processes of sex chromosome differentiation [11,[40][41][42][43]. Both plants and animals have accumulated TEs and satDNAs in the nonrecombining regions of Y and W chromosomes [11,40,[42][43][44][45][46]. Studies on neo-Y chromosomes of several Drosophila species proposed that the first steps of Y chromosome degeneration are driven by accumulation of TEs and satDNAs [41,45]. ...
... Although the difference in the extent of repeat expansion/contraction may be related to demographic history [92,93], it may have had a critical role in the evolution of the distinct karyotypes. Both TEs and satDNAs affect sex chromosome evolution and differentiation after recombination is halted, TEs likely affecting the formation of satDNAs and the conversion of euchromatic chromosomes into heterochromatic ones [11,[40][41][42][43][44][45][46]. Finally, the evolutionary young origin of diverse karyotypes, together with multiple emergences of neo-sex chromosomes place the morabine grasshoppers of the viatica species group in a pivotal position to address the impact of the repeatome on the evolution of different genomic architectures. ...
Comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats
Article
Full-text available
Background Repetitive DNA sequences, including transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), collectively called the “repeatome”, are found in high proportion in organisms across the Tree of Life. Grasshoppers have large genomes, averaging 9 Gb, that contain a high proportion of repetitive DNA, which has hampered progress in assembling reference genomes. Here we combined linked-read genomics with transcriptomics to assemble, characterize, and compare the structure of repetitive DNA sequences in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex and determine their contribution to genome evolution. Results We obtained linked-read genome assemblies of 2.73–3.27 Gb from estimated genome sizes of 4.26–5.07 Gb DNA per haploid genome of the four chromosomal races of V. viatica. These constitute the third largest insect genomes assembled so far. Combining complementary annotation tools and manual curation, we found a large diversity of TEs and satDNAs, constituting 66 to 75% per genome assembly. A comparison of sequence divergence within the TE classes revealed massive accumulation of recent TEs in all four races (314–463 Mb per assembly), indicating that their large genome sizes are likely due to similar rates of TE accumulation. Transcriptome sequencing showed more biased TE expression in reproductive tissues than somatic tissues, implying permissive transcription in gametogenesis. Out of 129 satDNA families, 102 satDNA families were shared among the four chromosomal races, which likely represent a diversity of satDNA families in the ancestor of the V. viatica chromosomal races. Notably, 50 of these shared satDNA families underwent differential proliferation since the recent diversification of the V. viatica species complex. Conclusion This in-depth annotation of the repeatome in morabine grasshoppers provided new insights into the genome evolution of Orthoptera. Our TEs analysis revealed a massive recent accumulation of TEs equivalent to the size of entire Drosophila genomes, which likely explains the large genome sizes in grasshoppers. Despite an overall high similarity of the TE and satDNA diversity between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.
View
... The repeatome is involved in the processes of sex chromosome differentiation [11,[40][41][42][43]. Both plants and animals have accumulated TEs and satDNAs in the nonrecombining regions of Y and W chromosomes [11,40,[42][43][44][45][46]. ...
... The repeatome is involved in the processes of sex chromosome differentiation [11,[40][41][42][43]. Both plants and animals have accumulated TEs and satDNAs in the nonrecombining regions of Y and W chromosomes [11,40,[42][43][44][45][46]. Studies on neo-Y chromosomes of several Drosophila species proposed that the first steps of Y chromosome degeneration are driven by accumulation of TEs and satDNAs [41,45]. ...
... Although the difference in the extent of repeat expansion/contraction may be related to demographic history [92,93], it may have had a critical role in the evolution of the distinct karyotypes. Both TEs and satDNAs affect sex chromosome evolution and differentiation after recombination is halted, TEs likely affecting the formation of satDNAs and the conversion of euchromatic chromosomes into heterochromatic ones [11,[40][41][42][43][44][45][46]. Finally, the evolutionary young origin of diverse karyotypes, together with multiple emergences of neo-sex chromosomes place the morabine grasshoppers of the viatica species group in a pivotal position to address the impact of the repeatome on the evolution of different genomic architectures. ...
Too much too many: comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats
Preprint
  • Aug 2020
Background The repeatome, the collection of repetitive DNA sequences represented by transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), is found in high proportion in organisms across the tree of life. Grasshoppers have large genomes (average 9 Gb), containing large amounts of repetitive DNA which has hampered progress in assembling reference genomes. Here we combined linked-read genomics with transcriptomics to assemble, characterize, and compare the structure of the repeatome and its contribution to genome evolution, in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex. Results We obtained linked-read genome assemblies of 2.73-3.27 Gb from estimated genome sizes of 4.26-5.07 Gb DNA per haploid genome of the four chromosomal races of V. viatica . These constitute the third largest insect genomes assembled so far (the largest being two locust grasshoppers). Combining complementary annotation tools and manual curation, we found a large diversity of TEs and satDNAs constituting 66 to 75 % per genome assembly. A comparison of sequence divergence within the TE classes revealed massive accumulation of recent TEs in all four races (314-463 Mb per assembly), indicating that their large genome size is likely due to similar rates of TE accumulation across the four races. Transcriptome sequencing showed more biased TE expression in reproductive tissues than somatic tissues, implying permissive transcription in gametogenesis. Out of 129 satDNA families, 102 satDNA families were shared among the four chromosomal races, which likely represent a repertoire of satDNA families in the ancestor of the V. viatica chromosomal races. Notably, 50 of these shared satDNA families underwent differential proliferation since the recent diversification of the V. viatica species complex. Conclusion In-depth annotation of the repeatome in morabine grasshoppers provided new insights into the genome evolution of Orthoptera. Our TEs analysis revealed a massive recent accumulation of TEs equivalent to the size of entire Drosophila genomes, which likely explains the large genome sizes in grasshoppers. Although the TE and satDNA repertoires were rather similar between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.
View
... This accumulation is transient because transposable elements may increase the instances of chromosome breaks (Charlesworth et al. 2005;Bachtrog 2013) or insert into coding and regulatory regions of the Y chromosome, inactivating genes. Both lead to eventual loss of genes and gene function (Matsunaga 2009). These changes, along with the differential selection on the X and Y, will result in permanent chromosomal heterozygosity (Muller 1918;Charlesworth et al. 2005;Bachtrog 2013). ...
... This increase in size probably occurs with the inevitable initial inflation of the Y with transposable elements, as is the case in the Drosophila miranda neo-Y chromosome. In addition to interacting with the common element A found in Drosophila sex chromosomes, the neo-Y system in D. miranda is hypothesized to have been formed by a Y-autosome fusion with Muller elements C and D, about 1.2 million years ago (Bachtrog et al. 2008;Matsunaga 2009;Mahajan et al. 2018). This chromosome still harbors many functional genes, yet has more than 20-fold greater accumulation of repetitive sequences than the X chromosome (Bachtrog et al. 2008). ...
Genome Size Evolution within and between the Sexes
Article
Full-text available
  • Nov 2018
Genome sizes are known to vary between closely related species, but the patterns behind this variation have yet to be fully understood. While this variation has been evaluated between species and within sexes, unknown is the extent to which this variation is driven by differentiation in sex-chromosomes. In order to address this longstanding question, we examine the mode and tempo of genome size evolution for a total of 87 species of Drosophilidae, estimating and updating male genome size values for 44 of these species. We compare the evolution of genome size within each sex to the evolution of the differences between the sexes. Utilizing comparative phylogenetic methods, we find that male and female genome size evolution is largely a neutral process, reflective of phylogenetic relatedness between species, which supports the newly proposed accordion model for genome size change. When similarly analyzed, the difference between the sexes due to heteromorphic sex chromosomes is a dynamic process; the male-female genome size difference increases with time with or without known neo-Y events or complete loss of the Y. Observed instances of rapid change match theoretical expectations and known neo-Y and Y loss events in individual species.
View
... The Y chromosome of P. phalangioides is reported to be formed exclusively by constitutive heterochromatin [31]. Therefore, an enlargement of the Y chromosome in this spider could be ascribed to considerable accumulation of repetitive sequences, which usually predominate in constitutive heterochromatin [67,79,80]. Cases of enlargement of sexlimited sex chromosomes due to repetitive DNA accumulation are known in several organisms [8,45,[81][82][83][84][85][86][87][88]. ...
Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation
Article
Full-text available
  • Jul 2020
Spiders are an intriguing model to analyse sex chromosome evolution because of their peculiar multiple X chromosome systems. Y chromosomes were considered rare in this group, arising after neo-sex chromosome formation by X chromosome-autosome rearrangements. However, recent findings suggest that Y chromosomes are more common in spiders than previously thought. Besides neo-sex chromosomes, they are also involved in the ancient X1X2Y system of haplogyne spiders, whose origin is unknown. Furthermore, spiders seem to exhibit obligatorily one or two pairs of cryptic homomorphic XY chromosomes (further cryptic sex chromosome pairs, CSCPs), which could represent the ancestral spider sex chromosomes. Here, we analyse the molecular differentiation of particular types of spider Y chromosomes in a representative set of ten species by comparative genomic hybridisation (CGH). We found a high Y chromosome differentiation in haplogyne species with X1X2Y system except for Loxosceles spp. CSCP chromosomes exhibited generally low differentiation. Possible mechanisms and factors behind the observed patterns are discussed. The presence of autosomal regions marked predominantly or exclusively with the male or female probe was also recorded. We attribute this pattern to intraspecific variability in the copy number and distribution of certain repetitive DNAs in spider genomes, pointing thus to the limits of CGH in this arachnid group. In addition, we confirmed nonrandom association of chromosomes belonging to particular CSCPs at spermatogonial mitosis and spermatocyte meiosis and their association with multiple Xs throughout meiosis. Taken together, our data suggest diverse evolutionary pathways of molecular differentiation in different types of spider Y chromosomes.
View
... Sex chromosomes are some of the most dynamic parts of genomes, including their repetitive DNA content (Steinemann and Steinemann 2005;Graves 2008;Matsunaga 2009;Hobza et al. 2017). Across diverse taxa, these chromosomes have originated independently from ordinary pairs of autosomes during evolution, but they present similar evolutionary fates (Bachtrog et al. 2011;Bachtrog 2013;Wright et al. 2016;Charlesworth 2017). ...
High dynamism for neo-sex chromosomes: satellite DNAs reveal complex evolution in a grasshopper
Article
Full-text available
  • Jun 2020
A common characteristic of sex chromosomes is the accumulation of repetitive DNA, which accounts for their diversification and degeneration. In grasshoppers, the X0 sex-determining system in males is considered ancestral. However, in some species, derived variants like neo-XY in males evolved several times independently by Robertsonian translocation. This is the case of Ronderosia bergii, in which further large pericentromeric inversion in the neo-Y also took place, making this species particularly interesting for investigating sex chromosome evolution. Here, we characterized the satellite DNAs (satDNAs) and transposable elements (TEs) of the species to investigate the quantitative differences in repeat composition between male and female genomes putatively associated with sex chromosomes. We found a total of 53 satDNA families and 56 families of TEs. The satDNAs were 13.5% more abundant in males than in females, while TEs were just 1.02% more abundant in females. These results imply differential amplification of satDNAs on neo-Y chromosome and a minor role of TEs in sex chromosome differentiation. We showed highly differentiated neo-XY sex chromosomes owing to major amplification of satDNAs in neo-Y. Furthermore, chromosomal mapping of satDNAs suggests high turnover of neo-sex chromosomes in R. bergii at the intrapopulation level, caused by multiple paracentric inversions, amplifications, and transpositions. Finally, the species is an example of the action of repetitive DNAs in the generation of variability for sex chromosomes after the suppression of recombination, and helps understand sex chromosome evolution at the intrapopulation level.
View
... Species with young sex chromosomes are expected to have similar female and male genome sizes, as the sex chromosomes are less differentiated. Early in differentiation of these sex chromosomes, the Y chromosome is expected to increase in size and become more heterochromatized due to increased mobile element activity and loss of genic content (Fig. 2) (Charlesworth et al. 2005;Matsunaga 2009;Bachtrog 2013). It is then expected that the Y chromosome will continue to become heterochromatized as it subsequently degrades due to transposable element suppression and deletion bias (Fig. 2). ...
Thoracic underreplication in Drosophila species estimates a minimum genome size and the dynamics of added DNA
Article
  • May 2020
Many cells in the thorax of Drosophila were found to stall during replication, a phenomenon known as underreplication. Unlike underreplication in nuclei of salivary and follicle cells, this stall occurs with less than one complete round of replication. This stall point allows precise estimations of early‐replicating euchromatin and late‐replicating heterochromatin regions, providing a powerful tool to investigate the dynamics of structural change across the genome. We measure underreplication in 132 species across the Drosophila genus and leverage this data to propose a model for estimating the rate at which additional DNA is accumulated as heterochromatin and euchromatin and also predict the minimum genome size for Drosophila . According to comparative phylogenetic approaches, the rates of change of heterochromatin differ strikingly between Drosophila subgenera. While these subgenera differ in karyotype, there were no differences by chromosome number, suggesting other structural changes may influence accumulation of heterochromatin. Measurements were taken for both sexes, allowing the visualization of genome size and heterochromatin changes for the hypothetical path of XY sex chromosome differentiation. Additionally, the model presented here estimates a minimum genome size in Sophophora remarkably close to the smallest insect genome measured to date, in a species over 200 million years diverged from Drosophila . This article is protected by copyright. All rights reserved
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... Evolutionary forces lead to a great variation in the copy number and types of heterochromatin repeats between closely related species. As repetitive DNA elements replicate, mechanisms such as unequal crossover, rolling circle replication, and segmental duplication become sources of genome evolution [68,69]. Thus, our study supports observations from other organisms that sex chromosomes have a propensity to accumulate species-specific differences in heterochromatin [70]. ...
Structural Variation of the X Chromosome Heterochromatin in the Anopheles gambiae Complex
Article
Full-text available
  • Mar 2020
Heterochromatin is identified as a potential factor driving diversification of species. To understand the magnitude of heterochromatin variation within the Anopheles gambiae complex of malaria mosquitoes, we analyzed metaphase chromosomes in An. arabiensis, An. coluzzii, An. gambiae, An. merus, and An. quadriannulatus. Using fluorescence in situ hybridization (FISH) with ribosomal DNA (rDNA), a highly repetitive fraction of DNA, and heterochromatic Bacterial Artificial Chromosome (BAC) clones, we established the correspondence of pericentric heterochromatin between the metaphase and polytene X chromosomes of An. gambiae. We then developed chromosome idiograms and demonstrated that the X chromosomes exhibit qualitative differences in their pattern of heterochromatic bands and position of satellite DNA (satDNA) repeats among the sibling species with postzygotic isolation, An. arabiensis, An. merus, An. quadriannulatus, and An. coluzzii or An. gambiae. The identified differences in the size and structure of the X chromosome heterochromatin point to a possible role of repetitive DNA in speciation of mosquitoes. We found that An. coluzzii and An. gambiae, incipient species with prezygotic isolation, share variations in the relative positions of the satDNA repeats and the proximal heterochromatin band on the X chromosomes. This previously unknown genetic polymorphism in malaria mosquitoes may be caused by a differential amplification of DNA repeats or an inversion in the sex chromosome heterochromatin.
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... In fishes, tandem or dispersed repetitive DNA sequences are relevant markers for clarifying karyotype evolution and sex chromosome differentiation (Schemberger et al. 2011, Barbosa et al. 2017, do Nascimento et al. 2018, Glugoski et al. 2018. Their accumulation is a key factor for the morphogenesis and the differentiation process of sex chromosomes, and the induction of gene erosion (Matsunaga 2009, Schemberger et al. 2014, Ziemniczak et al. 2014). Despite the highly conserved karyotype structure, the genomes of Characidium species display a dynamic pattern of their internal chromosomal composition (Table 1, Fig. 2). ...
The karyotypes and evolution of ZZ/ZW sex chromosomes in the genus Characidium (Characiformes, Crenuchidae)
Article
Full-text available
  • Oct 2018
Available data on cytotaxonomy of the genus Characidium Reinhardt, 1867, which contains the greatest number of species in the Characidiinae (Crenuchidae), with 64 species widely distributed throughout the Neotropical region, were summarized and reviewed. Most Characidium species have uniform diploid chromosome number (2n) = 50 and karyotype with 32 metacentric (m) and 18 submetacentric (sm) chromosomes. The maintenance of the 2n and karyotypic formula in Characidium implies that their genomes did not experience large chromosomal rearrangements during species diversification. In contrast, the internal chromosomal organization shows a dynamic differentiation among their genomes. Available data indicated the role of repeated DNA sequences in the chromosomal constitution of the Characidium species, particularly, in sex chromosome differentiation. Karyotypes of the most Characidium species exhibit a heteromorphic ZZ/ZW sex chromosome system. The W chromosome is characterized by high rates of repetitive DNA accumulation, including satellite, microsatellite, and transposable elements (TEs), with a varied degree of diversification among species. In the current review, the main Characidium cytogenetic data are presented, highlighting the major features of its karyotype and sex chromosome evolution. Despite the conserved karyotypic macrostructure with prevalent 2n = 50 chromosomes in Characidium , herein we grouped the main cytogenetic information which led to chromosomal diversification in this Neotropical fish group.
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... The lack of recombination between X and Y chromosomes leads, among others, to accumulation of repetitive sequences and heterochromatinization of Y chromosome (Matsunaga 2009). This is not the rule in all plants with heteromorphic sex chromosomes, but in R. hastatulus, the original Y chromosome occurring in T race is strongly heterochromatinized (it shows numerous DAPI-positive bands all over its length). ...
Testing the translocation hypothesis and Haldane’s rule in Rumex hastatulus
Article
Full-text available
The translocation hypothesis regarding the origin of the XX/XY1Y2 sex chromosome system was tested with reference to the F1 hybrids between two chromosomal races of Rumex hastatulus. The hybrids derived from reciprocal crossing between the Texas (T) race and the North Carolina (NC) race were investigated for the first time with respect to the meiotic chromosome configuration in the pollen mother cells, pollen viability, and sex ratio. A sex chromosome trivalent in the NC × T males and two sex chromosome bivalents in the T × NC males were detected. The observed conjugation patterns confirmed the autosomal origin of the extra chromosome segments occurring in the North Carolina neo-sex chromosomes. Decreased pollen viability was found in the T × NC hybrid in contrast to the NC × T hybrid and the parental forms. Moreover, only in the T × NC hybrid sex ratio was significantly female-biased (1:1.72). Thus, Haldane's rule for both male fertility and male rarity was shown in this hybrid. According to the authors' knowledge, R. hastatulus is just the second plant with sex chromosomes in which Haldane's rule was evidenced.
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... This differential accumulation could be documented, for example, by Rber59, Rber61, Rber370, Rber491, Rber520 sequences that are accumulated in the centromere of neo-X, but they are absent in the neo-Y; as well as by accumulation of Rber158 in neo-Y and the exclusive observation of Rber248 and Rber299 in the neo-Y. Differential patterns concerning the accumulation of repetitive DNAs and heterochromatinization are common hallmark of many sex chromosome systems with suppressed recombination [9,[64][65][66][67][68], and were reported in several well studied insect species, such as in the Y of Drosophila melanogaster [69] and D. miranda [66] and in the W chromosomes of many lepidopteran species (e.g. [70]). ...
Uncovering the evolutionary history of neo-XY sex chromosomes in the grasshopper Ronderosia bergii (Orthoptera, Melanoplinae) through satellite DNA analysis
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Background: Neo-sex chromosome systems arose independently multiple times in evolution, presenting the remarkable characteristic of repetitive DNAs accumulation. Among grasshoppers, occurrence of neo-XY was repeatedly noticed in Melanoplinae. Here we analyzed the most abundant tandem repeats of R. bergii (2n = 22, neo-XY♂) using deep Illumina sequencing and graph-based clustering in order to address the neo-sex chromosomes evolution. Results: The analyses revealed ten families of satDNAs comprising about ~1% of the male genome, which occupied mainly C-positive regions of autosomes. Regarding the sex chromosomes, satDNAs were recorded within centromeric or interstitial regions of the neo-X chromosome and four satDNAs occurred in the neo-Y, two of them being exclusive (Rber248 and Rber299). Using a combination of probes we uncovered five well-defined cytological variants for neo-Y, originated by multiple paracentric inversions and satDNA amplification, besides fragmented neo-Y. These neo-Y variants were distinct in frequency between embryos and adult males. Conclusions: The genomic data together with cytogenetic mapping enabled us to better understand the neo-sex chromosome dynamics in grasshoppers, reinforcing differentiation of neo-X and neo-Y and revealing the occurrence of multiple additional rearrangements involved in the neo-Y evolution of R. bergii. We discussed the possible causes that led to differences in frequency for the neo-Y variants between embryos and adults. Finally we hypothesize about the role of DNA satellites in R. bergii as well as putative historical events involved in the evolution of the R. bergii neo-XY.
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The genome sequence of Drosophila melanogaster
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Full-text available
  • Jan 2000
The fly Drosophila melanogaster is one of the most intensively studied organisms in biology and serves as a model system for the investigation of many developmental and cellular processes common to higher eukaryotes, including humans. We have determined the nucleotide sequence of nearly all of the approximately 120-megabase euchromatic portion of the Drosophila genome using a whole-genome shotgun sequencing strategy supported by extensive clone-based sequence and a high-quality bacterial artificial chromosome physical map. Efforts are under way to close the remaining gaps; however, the sequence is of sufficient accuracy and contiguity to be declared substantially complete and to support an initial analysis of genome structure and preliminary gene annotation and interpretation. The genome encodes approximately 13,600 genes, somewhat fewer than the smaller Caenorhabditis elegans genome, but with comparable functional diversity.
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The Genome Sequence of Drosophila melanogaster
Article
Full-text available
  • Mar 2000
The fly Drosophila melanogaster is one of the most intensively studied organisms in biology and serves as a model system for the investigation of many developmental and cellular processes common to higher eukaryotes, including humans. We have determined the nucleotide sequence of nearly all of the ∼120-megabase euchromatic portion of theDrosophila genome using a whole-genome shotgun sequencing strategy supported by extensive clone-based sequence and a high-quality bacterial artificial chromosome physical map. Efforts are under way to close the remaining gaps; however, the sequence is of sufficient accuracy and contiguity to be declared substantially complete and to support an initial analysis of genome structure and preliminary gene annotation and interpretation. The genome encodes ∼13,600 genes, somewhat fewer than the smaller Caenorhabditis elegansgenome, but with comparable functional diversity.
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Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system
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Full-text available
  • Apr 2007
Y chromosomes are different from other chromosomes because of a lack of recombination. Until now, complete sequence information of Y chromosomes has been available only for some primates, although considerable information is available for other organisms, e.g., several species of Drosophila. Here, we report the gene organization of the Y chromosome in the dioecious liverwort Marchantia polymorpha and provide a detailed view of a Y chromosome in a haploid organism. On the 10-Mb Y chromosome, 64 genes are identified, 14 of which are detected only in the male genome and are expressed in reproductive organs but not in vegetative thalli, suggesting their participation in male reproductive functions. Another 40 genes on the Y chromosome are expressed in thalli and male sexual organs. At least six of these genes have diverged X-linked counterparts that are in turn expressed in thalli and sexual organs in female plants, suggesting that these X- and Y-linked genes have essential cellular functions. These findings indicate that the Y and X chromosomes share the same ancestral autosome and support the prediction that in a haploid organism essential genes on sex chromosomes are more likely to persist than in a diploid organism. • bryophyte • dioecy • Marchantia polymorpha
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Variation in genomic recombination rates among animal taxa and the case of social insects
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Meiotic recombination is almost universal among sexually reproducing organisms. Because the process leads to the destruction of successful parental allele combinations and the creation of novel, untested genotypes for offspring, the evolutionary forces responsible for the origin and maintenance of this counter-intuitive process are still enigmatic. Here, we have used newly available genetic data to compare genome-wide recombination rates in a report on recombination rates among different taxa. In particular, we find that among the higher eukaryotes exceptionally high rates are found in social Hymenoptera. The high rates are compatible with current hypotheses suggesting that sociality in insects strongly selects for increased genotypic diversity in worker offspring to either meet the demands of a sophisticated caste system or to mitigate against the effects of parasitism. Our findings might stimulate more detailed research for the comparative study of recombination frequencies in taxa with different life histories or ecological settings and so help to understand the causes for the evolution and maintenance of this puzzling process.
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Kejnovsk E, Hobza R, Cerm??k T, Kub??t Z, Vyskot B. The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102: 533-541
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  • Apr 2009
Eukaryotic genomes contain a large proportion of repetitive DNA sequences, mostly transposable elements (TEs) and tandem repeats. These repetitive sequences often colonize specific chromosomal (Y or W chromosomes, B chromosomes) or subchromosomal (telomeres, centromeres) niches. Sex chromosomes, especially non-recombining regions of the Y chromosome, are subject to different evolutionary forces compared with autosomes. In non-recombining regions of the Y chromosome repetitive DNA sequences are accumulated, representing a dominant and early process forming the Y chromosome, probably before genes start to degenerate. Here we review the occurrence and role of repetitive DNA in Y chromosome evolution in various species with a focus on dioecious plants. We also discuss the potential link between recombination and transposition in shaping genomes.
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Greeff JM, Van Vuuren GJJ, Kryger P, Moore JC. Outbreeding and possibly inbreeding depression in a pollinating fig wasp with a mixed mating system. Heredity 102: 349-356
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  • Mar 2009
Mixed mating systems are somewhat of an enigma as most models predict that organisms should either inbreed when inbreeding depression is low, or outbreed when inbreeding depression is high. Many wasps mix routine inbreeding with a little random mating. This random mating is most common when all local sibmating opportunities are exhausted and dispersal is the only way males can further increase their fitness. The males of the pollinating fig wasp, Platyscapa awekei, are slightly different in that they disperse before all sibmating opportunities have been exhausted. To see if this is a response to inbreeding depression we quantify inbreeding depression by comparing females' life time reproductive success to their heterozygosity at multiple microsatellite loci. We find that a female wasp's heterozygosity is an accurate predictor of her inbreeding coefficient and that P. awekei females actually seem to suffer from outbreeding depression and possibly from a little inbreeding depression. Male dispersal is thus not a means to effect the optimal mating system, but more likely a mechanism to reduce competition among brothers. The number of mature offspring a female produces depends on her own heterozygosity and not on that of the offspring, and may be determined by egg and gall quality.
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Low conservation of gene content in the Drosophila Y chromosome
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Chromosomal organization is sufficiently evolutionarily stable that large syntenic blocks of genes can be recognized even between species as distantly related as mammals and puffer fish (450 million years (Myr) of divergence). In Diptera, the gene content of the X chromosome and the autosomes is well conserved: in Drosophila more than 95% of the genes have remained on the same chromosome arm in the 12 sequenced species (63 Myr of divergence, traversing 400 Myr of evolution), and the same linkage groups are clearly recognizable in mosquito genomes (260 Myr of divergence). Here we investigate the conservation of Y-linked gene content among the 12 sequenced Drosophila species. We found that only a quarter of the Drosophila melanogaster Y-linked genes (3 out of 12) are Y-linked in all sequenced species, and that most of them (7 out of 12) were acquired less than 63 Myr ago. Hence, whereas the organization of other Drosophila chromosomes traces back to the common ancestor with mosquitoes, the gene content of the D. melanogaster Y chromosome is much younger. Gene losses are known to have an important role in the evolution of Y chromosomes, and we indeed found two such cases. However, the rate of gene gain in the Drosophila Y chromosomes investigated is 10.9 times higher than the rate of gene loss (95% confidence interval: 2.3-52.5), indicating a clear tendency of the Y chromosomes to increase in gene content. In contrast with the mammalian Y chromosome, gene gains have a prominent role in the evolution of the Drosophila Y chromosome.
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Sex Determination by Sex Chromosomes in Dioecious Plants
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: Sex chromosomes have been reported in several dioecious plants. The most general system of sex determination with sex chromosomes is the XY system, in which males are the heterogametic sex and females are homogametic. Genetic systems in sex determination are divided into two classes including an X chromosome counting system and an active Y chromosome system. Dioecious plants have unisexual flowers, which have stamens or pistils. The development of unisexual flowers is caused by the suppression of opposite sex primordia. The expression of floral organ identity genes is different between male and female flower primordia. However, these floral organ identity genes show no evidence of sex chromosome linkage. The Y chromosome of Rumex acetosa contains Y chromosome-specific repetitive sequences, whereas the Y chromosome of Silene latifolia has not accumulated chromosome-specific repetitive sequences. The different degree of Y chromosome degeneration may reflect on evolutionary time since the origination of dioecy. The Y chromosome of S. latifolia functions in suppression of female development and initiation and completion of anther development. Analyses of mutants suggested that female suppressor and stamen promoter genes are localized on the Y chromosome. Recently, some sex chromosome-linked genes were isolated from flower buds of S. latifolia.
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Complete Transfer of Perceptual Learning across Retinal Locations Enabled by Double Training
Article
  • Dec 2008
Practice improves discrimination of many basic visual features, such as contrast, orientation, and positional offset. Perceptual learning of many of these tasks is found to be retinal location specific, in that learning transfers little to an untrained retinal location. In most perceptual learning models, this location specificity is interpreted as a pointer to a retinotopic early visual cortical locus of learning. Alternatively, an untested hypothesis is that learning could occur in a central site, but it consists of two separate aspects: learning to discriminate a specific stimulus feature ("feature learning"), and learning to deal with stimulus-nonspecific factors like local noise at the stimulus location ("location learning"). Therefore, learning is not transferable to a new location that has never been location trained. To test this hypothesis, we developed a novel double-training paradigm that employed conventional feature training (e.g., contrast) at one location, and additional training with an irrelevant feature/task (e.g., orientation) at a second location, either simultaneously or at a different time. Our results showed that this additional location training enabled a complete transfer of feature learning (e.g., contrast) to the second location. This finding challenges location specificity and its inferred cortical retinotopy as central concepts to many perceptual-learning models and suggests that perceptual learning involves higher nonretinotopic brain areas that enable location transfer.
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