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Transcript
Biological Journal of the Linnean Society, 2010, 100, 737–752. With 3 figures
REVIEW ARTICLE
Sex chromosomes and sex determination pathway
dynamics in plant and animal models
BOHUSLAV JANOUSEK* and MARTINA MRACKOVA
Institute of Biophysics, Kralovopolska 135, Brno, CZ 612 65, Czech Republic
Received 23 November 2009; revised 17 March 2010; accepted for publication 17 March 2010
bij_1470
737..752
In this review, we discuss and compare data obtained from animal and plant models, focusing our attention on the
mechanisms that affect sex linkage and changes in sex-determining pathways. Patterns in data across taxa suggest
that sex bias and the dynamics that occurs within hybrid zones can play an important role in these processes that
enable the spread of some otherwise handicapped genotypes. We discuss the data obtained from several main plant
model species in the light of the patterns demonstrated in animal models. In several plant models, we discuss
possible differences in the age of their sex-determining pathways and the age of their current sex chromosomes.
We also address an open question: how can an X/A ratio based sex-determining system evolve from a sexdetermining system based on two genes on the Y chromosome that control two separate sex-determining pathways
(for the control of gynoecium suppression and anther promotion)? Taking inspiration from the well described
mechanisms involved in sex determination dynamics in animals, we suggest a hypothetical stepwise scenario of
change of the plant sex-determining system based on two separate sex-determining pathways (for the control of
gynoecium suppression and anther promotion) into the other sex-determining systems. We suppose that an
intermediate step occurs before shift to X/A based sex determination. At that phase, sex determination in plants
is still based on an active Y chromosome, although there exists already a connected control of both sex-determining
pathways. We suggest that this connection is enabled by the existence of the genes that control sexual dimorphism
in the vegetative state of plant development, and that, in some circumstances, these genes can become sexdetermining genes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100,
737–752.
ADDITIONAL KEYWORDS: evolution – hybrid zones – sexual dimorphism.
INTRODUCTION
The mechanisms involved in sex determination are
some of the most dynamic from an evolutionary point
of view. Gonochorism prevails in current animal model
species, although hermaphroditism is prevalent in
angiosperm plants (approximately 90%). However,
many plant families also include dioecious species, and
dioecy is present in several crop species (Grant et al.,
1994).
The sex chromosomes in plants and animals have
evolved independently, although the mechanisms of
*Corresponding author. E-mail: [email protected]
their evolution are probably very similar. The necessity of a synthesis of data obtained from various model
species can be demonstrated by considering the
research of the stepwise arrest of sex chromosome
recombination. In general, it is hypothesized that sex
chromosomes evolved from a specific pair of autosomes
carrying some sex-determining gene(s). Subsequently,
the newly-formed sex chromosomes stopped recombination in a small region around the sex-determining
locus. Sex chromosomes in this early stage of evolution are not cytologically distinguishable (homomorphic). The process of recombination suppression
then progresses through almost the entire sex chromosome. The results of the human genome project have
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
737
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B. JANOUSEK and M. MRACKOVA
revealed a correlation between the localization of
genes along the X chromosome and silent site
sequence divergence from their Y homologues. This
silent site sequence divergence serves as a measure
of the time since the X and Y copy stopped recombining. The regions containing genes with similar
levels of divergence were named ‘evolutionary strata’
based on a metaphorical similarity to geological
strata (Lahn & Page, 1999). Originally, the differences in silent site sequence divergence were
explained by several large chromosome rearrangements (Lahn & Page, 1999), although later research
showed that the boundaries between some strata are
blurred in mammals, suggesting that epigenetic
mechanisms or small inversions should also be taken
into account (Skaletsky et al., 2003). However, discrete strata, suggesting the role of chromosomal rearrangements in the arrest of recombination in birds,
were identified in chickens (Nam & Ellegren, 2008).
In humans, computer simulations of inversions followed by the analysis of putative breakpoints conducted by Lemaitre et al. (2009) indicate that
inversions played a crucial role in the origin of strata
4 and 5. Unfortunately, it was not possible to obtain
clear results for stratum 3 because its age precludes
successful use of the method. Results from nonvertebrate models suggest that the stepwise spread of a
nonrecombining region is generally widespread
process, probably connected with the existence of any
nonrecombining region. Gradients in the silent site
divergence have been found in plants (Silene latifolia; Nicolas et al., 2005) and fungi (Microbotryum
violaceum; Votintseva & Filatov, 2009). The dioecious
plant S. latifolia has much younger sex chromosomes
compared to humans but the strata are already
present in these chromosomes (Nicolas et al., 2005;
Bergero et al., 2007), which suggests that S. latifolia
is a promising model for the study of the initial
mechanisms of recombination arrest. Despite substantial progress in the knowledge of sex chromosome evolution, there are still topics that are not well
understood. One of them is why sex determination
(including sex determination systems on a chromosomal level) is conserved in some taxonomic groups,
whereas, in others, it is highly dynamic. In this
review, we present the current status of knowledge of
sex determination and sex determination plasticity in
animal and plant models. We also discuss possible
causes of differences and similarities between animal
and angiosperm models.
We then suggest a possible model of shifts in the
sex-determining systems in plants from a typical
plant sex determination system evolved from gynodioecy (Charlesworth & Charlesworth, 1978) into sexdetermining systems more similar to the systems
found in animal models.
SEX DETERMINATION PATHWAYS AND SEX
CHROMOSOME DYNAMICS IN ANIMALS
THE VARIABILITY OF SEX CHROMOSOMES AND
SEX-DETERMINING PATHWAYS IN INSECTS
Sex-determining systems in insects exhibit a
wide range of diversity. In addition to XX/XY and
ZW/ZZ sex-determining systems, some taxa have
evolved systems that have not been found in any
other classes: for example, the haploid/diploid sexdetermining system or, more exactly, the complementary sex-determining system, present in social insects
such as Hymenoptera and Isoptera (Sánchez, 2008).
Surprising findings from recent years point to a
common origin of these extremely diverse sexdetermining systems. The role of the doublesex gene is
evolutionary well conserved even in species with
complementary sex determination (Sánchez, 2008).
The doublesex (dsx) gene was originally described in
Drosophila melanogaster. It is involved in the control
of somatic sexual differentiation in both sexes. Two
functional products are encoded by dsx: one product is
expressed in females and represses male differentiation, and the other is expressed in males and represses
female differentiation (Burtis & Baker, 1989). In the
order Diptera (most often studied), the prevailing
sex-determining systems are of the XX/XY type (either
with the active role of the Y-chromosome or X/A ratio
based). These systems diversified into different types
of sex determination based on the selective elimination
of paternal chromosomes in some fraction of offspring.
In at least one species, Musca domestica, extreme
variability and plasticity of the sex determination is
present. Sex linkage change is controlled by the presence of the gene modifier M, which transforms individuals without the Y chromosome into males. In some
populations, this modifier is fixed and sex determination is under the control of another unlinked gene, FD,
which causes females to arise even in the presence of
the male factor. This sex linkage change is therefore
connected with the switch to female heterogamety
(Dübendorfer et al., 2002). In the main Dipteran model
species, D. melanogaster, this extent of sex determination plasticity is not present. In this species, the
probable role of dosage compensation and Sex-lethalbased sex determination was suggested by Schütt &
Nöthiger (2000) as an explanation of the stability of sex
determination. Sex-lethal (Sxl) is a master gene that
regulates the splicing of doublesex, so that its early
expression in females (based on the X/A ratio) leads to
a female type of doublesex splicing (Bell et al., 1988).
Simultaneously, this early expression of Sex-lethal in
females prevents the expression of male-specific lethal
2 (msl-2) that controls dosage compensation by doubling the expression levels of the X-linked genes in D.
melanogaster males (McDowell, Hilfiker & Lucchesi,
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
SEX CHROMOSOMES AND SEX DETERMINATION PATHWAY DYNAMICS
1996). A great variability of the sex chromosomes is,
however, observed in the various species of the genus
Drosophila (Charlesworth & Charlesworth, 2005). In
Drosophila affinis, fertile male individuals without a Y
chromosome can be found (Voelker & Kojima, 1971).
The sex determination of another often studied order,
Lepidoptera, was ancestrally based on the ZO/ZZ
system. This system, however, evolved in many Lepidopteran species, including the main Lepidopteran
model Bombyx mori to the ZW/ZZ sex determination
system (Traut, Sahara & Marec, 2007).
The important mechanism for the spatial spread of
the novel sex chromosomes was revealed based on the
data obtained in grasshopper Podisma pedestris
(Veltsos, Keller & Nichols, 2008). In the hybrid zone,
the neo Y-chromosome can spread despite the harm
that it causes its carriers because sexually antagonistic effects of the neo-Y chromosome induce selection in
favour of the neo X-chromosomes causing their spread,
such that they simultaneously remove the original X
chromosome from the population. This selection then
helps to the neo Y-chromosome to spread in the population. Paradoxically, processes of Y-chromosome
degeneration can theoretically support its expansion in
metapopulations (Veltsos et al., 2008). This finding
suggests that hybrid zones can enable evolutionary
processes that would not be possible in a single
unstructured population. It is also possible to speculate that similar or related processes, with a different
focus of antagonistic selection, may explain the spread
of other types of chromosomal rearrangements considered to be subject to positive frequency-dependent
selection (Pannell & Pujol, 2009)
SEX-DETERMINING
SYSTEMS IN FISH AND THE
HYPOTHESES EXPLAINING THE DYNAMICS OF
SEX-DETERMINING PATHWAYS
Fish are an important group of models that have
undergone dynamic evolution in sex determination
pathways and sex determination. Sex determination in
fish is predominantly established by genotype but it
can be often influenced by environmental factors
(Baroiller, D’Cotta & Saillant, 2009). Although gonochorism is common, there are also several hundreds
of hermaphroditic species (Devlin & Nagahama, 2002).
Moreover, in some species, individuals undergo a
sex change (males to females or vice versa) during
their life in response to age, social factors or temperature (Schartl, 2004). The variability of the sexdetermining systems in fish is representented not only
by the presence of both of the two common heterogametic systems (XY male heterogamety and ZW female
heterogamety), but also by occurrence of several different modifications of these primary systems (e.g. in
genus Xiphophorus; Kallman, 1984). Recently, two
739
main model genera have been used in studies of sex
determination: Oryzias and Xiphophorus (especially
the species Xiphophorus maculatus). All known species
from the genus Oryzias belong to one of three phylogenetically distinct groups: latipes, javanicus, and
celebensis (Takehana, Naruse & Sakaizumi, 2005). The
species Oryzias latipes and Oryzias curvinotus from
the group latipes have an XY sex-determining system.
In these species, the sex-determining gene is DMY
(also called dmrt1bY, according to its origin from the
duplicated autosomal gene dmrt1; Matsuda et al.,
2002; Nanda et al., 2002; Matsuda et al., 2003).
However, this sex-determining gene is not present
in all Oryzias species. Genetic mapping has revealed
that different genes and different linkage groups are
involved in sex determination in the other two groups
(Kondo et al., 2003; Takehana et al., 2007a). Moreover,
the sex-determining system in Oryzias hubbsi, a
species from the javanicus group, is not XX/XY as in
closely-related Oryzias dancena, but ZZ/ZW (Takehana
et al., 2007b). Genetic mapping also showed that sex
chromosomes of O. hubbsi and O. dancena evolved
from different autosomal ancestors (Takehana et al.,
2007b).
Another remarkable model is the genus Xiphophorus (Schartl, 1995). Studies in this genus (Morizot
et al., 1991) revealed sex determination systems that
vary from simple XX/XY or ZZ/ZW systems to multifactorial sex determination (Volff & Schartl, 2001). The
species X. maculatus has an unusual sex-determining
system with three different homomorphic sex chromosomes: X, Y, and W (Kallman, 1984). Different combinations of sex chromosomes determine whether fish
become males or females: males have XY or YY, and
females have XX, WX or WY gonosomal pairs (Volff &
Schartl, 2001). Several models have attempted to
explain this three-chromosomes system. According to
Volff & Schartl (2001), each sex chromosome could
have a different copy number of genes ‘pushing’ the
development in male direction (male determining
gene): Y, two copies; X, one copy, and W, no copies.
According to the number of sex-genes an individual
becomes male or female. The evolutionary events
leading to this type of sex determination system are
still unclear but, according to experimental data, it is
possible to surmise that the mechanisms of sexdetermining pathway evolution in fish are similar to
the mechanisms taking place in insects. According to
hypothesis of Ezaz et al. (2006), X. maculatus is caught
in a transition between the XY and ZW systems.
Quantitative basis of sex determination was recently
described also in related species Poecilia reticulata,
which becomes a widely studied model. Cross of the
individuals from different populations revealed the X
chromosomes differring in the strenght of their male
(respectively female) tendency. Male organ develop-
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
740
B. JANOUSEK and M. MRACKOVA
ment is therefore possible even in the absence of the Y
chromosome (Tripathi et al., 2009).
Schartl (2004) presented a theory explaining the
mechanisms the sex linkage change in fish that can
also be applied to other taxonomic groups. This theory
is derived from the theory of Wilkins (1995) concerning
the evolution of sex-determining cascades. Wilkins’
theory was deduced from the data obtained in Caenorhabditis elegans. Wilkins (1995) hypothesized that
the evolution of sex-determining cascades involves the
sequential acquisition of new gene functions in reverse
order (the last acquired gene function performs the
first step in the cascade). Schartl (2004) adopted the
theory of Wilkins (1995), but also stressed the role of
gene duplications in the evolution of sex-determining
pathways. According to Schartl’s theory, some of the
genes in the sex-determining pathway can be changed
into the master sex-determining gene by duplication.
Important progress in the theory of the turnover of
sex chromosomes was achieved by van Doorn &
Kirkpatrick (2007), who showed that sexually antagonistic autosomal gene can under some conditions
stimulate ‘hijacking’ of sex determination by a new sex
expression-influencing mutation that occurs in its
proximity. This process leads to the formation of the
neo-X and neo-Y from the autosome carrying sexually
antagonistic locus, whereas the original Y-chromosome
is lost from the population and the original X becomes
an autosome. The great evolutionary stability in some
taxonomic groups can be therefore explained by presence of the genes important for male fertility on the
original Y that are absent on the X, by the presence of
dosage compensation, and/or by the presence of the
sexualy antagonistic genes on the original sex chromosomes. The conditions for the hijacking of sex determination are then more restrictive. Sex-limited
expression can, however, lead to the loss of polymorphism at the ancestral sex chromosomes and make the
turnover of sex chromosomes easier.
THE
ROLE OF HYBRIDS ZONES IN THE PLASTICITY OF
SEX DETERMINATION AND DYNAMICS OF SEX
CHROMOSOMES: LESSONS FROM AMPHIBIANS
The role of sex bias in the evolution of sex-determining
pathways and sex chromosomes is exhibited in the
Japanese frog, Rana rugosa. This species forms population groups varying in type of heterogamety and
morphology of sex chromosomes. The main four groups
are named according to geographical locations (Fig. 1),
and a recently discovered group is called ‘Neo-ZW’
according to phylogeny (Ogata et al., 2008). Three of
them have the XX/XY sex determination system,
whereas the north-west Japan and the Neo-ZW show
female heterogamety (ZZ/ZW) (Miura et al., 1998;
Ogata et al., 2008). West Japan and Kanto groups have
Figure 1. Scheme explaining the role of sex bias in sex
linkage change and heteromorphic chromosome formation
in Rana rugosa. Big arrows show the sex and direction of
movement of individuals founding the derived populations.
The male bias in the north-west population is suppressed
by the newly arisen locus responsible for sex change (x to
W transformation). In the central population, the original
female bias is compensated for by the accumulation of
male advantageous genes on the original y chromosome
(y to Y transformation) (sensu Ogata et al., 2003).
cytologically indistinguishable sex chromosomes,
whereas central and north-west Japan groups possess
heteromorphic sex chromosomes (Miura et al., 1998).
According to sequence similarities, it can be deduced
that the chromosomes Y and Z originated from the
west Japan type of sex chromosomes, whereas X and W
originated from the Kanto type of sex chromosomes.
These results suggest that small group(s) of individuals were isolated geographically from the original
population and their sex chromosome evolution pathways diverged. Afterwards, these two groups (west
Japan and Kanto) could have met each other again and
reciprocally hybridized (Fig. 1). Subsequently, subpopulations of progeny could have been separated from
their parental populations and evolved independently.
This theory was experimentally tested by artificial
crossings between these ‘parental’ groups with homomorphic sex chromosomes (Ogata et al., 2003). The
crossings between west Japan females and Kanto
males produced progeny with a male-biased sex ratio,
whereas the reciprocal crossings produced progeny
with a female-biased sex ratio. These results suggest
that the sex bias could cause a strong positive selective
pressure for the minor sex-favouring gene to reestablish the 1 : 1 sex ratio. This hypothesis is also supported by the results of phylogenetic analysis based on
mitochondrial sequences. This example illustrates
that intense sex bias can promote accumulation of
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
SEX CHROMOSOMES AND SEX DETERMINATION PATHWAY DYNAMICS
sexually antagonistic genes, leading to formation of
heteromorphic sex chromosomes or even the acquisition of a new dominant sex determiner that caused the
evolution of a novel sex-determining system (ZW/ZZ).
These data well support the theoretical studies of van
Doorn & Kirkpatrick (2007).
SEX CHROMOSOMES AND PLASTICITY OF
SEX DETERMINATION IN MAIN PLANT
MODEL SPECIES
Although most angiosperm plant models are reported
as having stable genetically based sex-determining
systems, even in angiosperm plants, some cases of
nongenetic sex determination and fluctuating sex
occur (e.g. the genus Arisaema: Policansky, 1981;
Renner, Zhang & Murata, 2004). Moreover, even in
species with well established genetic sex determination, a certain level of instability of sexual phenotype
can be found (Shull, 1911; Winge, 1931; Ainsworth
et al., 2005).
The research of this problem in plants is rare in
comparison with animal models. So far, no cases of
change of XX/XY to ZW/ZZ system (or other sexdetermining system) have been described in plants.
Here, we present an overview of the data concerning
the plasticity of the sex chromosomes and sexdetermining pathways that were obtained in a main
angiosperm model species.
As described above, the sex-determining pathways
in animals (or at least in their large taxonomic units)
are highly conserved. In all chordates and lancelets,
sex organ differentiation is likely based on the action of
the sex steroid hormones (Mizuta & Kubokawa, 2007)
and their receptors (Baker & Chang, 2009) and, as
decribed above, a large proportion of invertebrates
have sex-determining pathways based on the gene
doublesex (Sánchez, 2008). On the other hand, dioecy
evolved independently in plants more than 100 times
to account for 160 plant families that include dioecious
species (Charlesworth and Guttman, 1999) and, thus,
it is very unlikely that the sex-determining pathways
in all dioecious plants are of the same origin. Moreover,
several different routes leading to dioecy have been
described: from hermaphroditism through gynodioecy
(Charlesworth & Charlesworth, 1978), from selfincompatibility through polyploidization (e.g. species
of the genus Lycium; Miller & Venable, 2000), and
directly from monoecy (e.g. species of the genus
Siparuna, Renner & Won, 2001). The evolutionary
routes to androdioecy are probably very rarely seen in
the nature. The route from hermaphroditism through
androdioecy is unlikely to evolve because the conditions for the invasion and spread of males among
hermaphrodites are severe (Charlesworth & Charles-
741
worth, 1978; Pannell, 2002). The most famous proposed example of this route, the genus Datisca, has not
been confirmed by more extensive phylogenetic studies
(Zhang et al., 2006). Similarly, the genus Acer as an
example of the route from heterodichogamy through
androdioecy (Pannell & Verdú, 2006) was not further
confirmed (Renner et al., 2007). A putative candidate
for the origin of the dioecy through androdioecy could
be subdioecious Fragaria virginiana (incipient ZW/ZZ
system), as indicated by the presence of the dominant
suppressor of male fertility on the proto-W chromosome and by the presence of the recessive allele
causing female sterility on the proto-Z chromosome
(Spigler et al., 2008; Moore, 2009). However, it is not
possible to reject the hypothesis that this status is
secondary unless extensive phylogenetic studies are
carried out.
Because of the frequently independent origin of
sex determination in individual plant families or even
genera, we discuss the topics of sex determination
plasticity and sex chromosome changes separately in
the chosen model genera and species.
SILENE
LATIFOLIA AND
SILENE
DIOICA: SPECIES
CONSIDERED TO HAVE STABLE SEX DETERMINATION
SHOW SOME PLASTICITY OF SEX EXPRESSION
A small cluster of dioecious species in the genus Silene
have evolved chromosomal sex determination and
sex chromosomes relatively recently, within the
last 10 Myr. Five dioecious Silene species (Silene
heuffelii, S. dioica, S. latifolia, Silene diclinis, and
Silene marizii; the former section Elisanthe) are very
closely related (1–2 Myr of divergence), and it was
previously considered that all five species had morphologically similar sex chromosomes (Nicolas et al.,
2005). Recently, neo-sex chromosomes originated by
reciprocal translocation between the original Y chromosome and an autosome were reported in S. diclinis
(Howell, Armstrong & Filatov, 2009).
Silene latifolia (Fig. 2A, B) is a widely studiedj
dioecious model. The mechanism of sex determination
in this species is based on the presence of three kinds
of genes that are located in the nonrecombining region
of the Y-chromosome: stamen promoting gene(s) [often
called stamen-promoting function to emphasize that
the exact molecular principle of its (or their) action is
not yet known] promote the development of anthers
and filaments (Donnison et al., 1996; Farbos et al.,
1999), male fertility gene(s) (called male fertility
function) enable the production of the fertile pollen
(Donnison et al., 1996; Farbos et al., 1999), and gynoecium suppressing gene(s) (often called gynoeciumsuppressing function) control the arrest of the
gynoecium development in males (Donnison et al.,
1996; Lardon et al., 1999).
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
742
B. JANOUSEK and M. MRACKOVA
A
B
C
D
Figure 2. Examples of two dioecious models from the genus Silene. A, Silene latifolia male. B, Silene latifolia female.
C, Silene colpophylla male. D, Silene colpophylla female.
A good illustration of the fact that even plant
species with a well established sex determination
system based on the active Y chromosome and with a
good phenotypic stability of the sexual phenotype
(van Nigtevecht, 1966) are prone to changes in sex
determination is the finding of a dominant autosomal
mutation in S. latifolia that causes transformation
of males to androhermaphrodites (Lardon et al.,
1999). The androhermaphroditism in S. latifolia can
be also induced by the action of the DNA hypomethylating (Janousek, Siroky & Vyskot, 1996; Janoušek,
Grant & Vyskot, 1998), or histone H4 hyperacetylating drugs (Zluvova et al., 2008a). The assumed
mechanism of these agents is DNA hypermethylation
of the Y-linked gynoecium suppressor that occurs as a
consequence of a genome hypomethylation (Janousek
et al., 1996; Janoušek et al., 1998). This hypermethylation is probably the result of defence mechanisms
that serve to inactivate transposable elements activated by overall DNA hypomethylation (or histone
hyperacetylation) (Zluvova et al., 2008a).
There are already some experimental data concerning the mechanism of gynoecium suppression in males.
Histological studies have revealed a reduction of cell
division in the central part of the male flower meristem
(Matsunaga, Uchida & Kawano, 2004). Molecular
studies have revealed the role of homologues of Arabi-
dopsis thaliana SHOOTMERISTEMLESS (STM) and
CUP SHAPED COTYLEDON (CUC) 1 and CUC2
genes in the arrest of the gynoecium development in S.
latifolia males (Zluvova et al., 2006). The data (Matsunaga et al., 2004; Zluvova et al., 2006) suggest that
an absence of SHOOTMERISTEMLESS (STM) and
the presence of CUP SHAPED COTYLEDON (CUC) 1
and CUC2 transcripts in the central part of the male
flower meristem are the cause of reduced meristematic
activity in this region. The results obtained by Kazama
et al. (2009) indicate a possible role of SUPERMANlike gene in the suppression of the anther development
in S. latifolia females.
Interestingly, some sex-specific differences in gene
expression patterns were detected in plants before
flowering, suggesting a hidden sexual dimorphism in
S. latifolia (Zluvova et al., 2008b; J. Zluvova, unpubl.
data). The existence of such a dimorphism is also
supported by the data showing quantitative differences between males and females in photosynthesis
(Gehring & Monson, 1994) and in other quantitative
traits (Laporte & Delph, 1995; Delph et al., 2005).
Because of the large number of the sexually dimorphic
traits, it is reasonable to suppose that a master gene(s)
for their control is located on the Y chromosome and
that autosomal genes with sex-limited expression are
involved in sexual dimorphism in S. latifolia.
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
SEX CHROMOSOMES AND SEX DETERMINATION PATHWAY DYNAMICS
SILENE,
SECTION
OTITES:
SEX LINKAGE CHANGE OR
INDEPENDENT EVOLUTION OF DIOECY?
Section Otites is a group of morphologically similar dioecious species (Wrigley, 1986) that are evolutionary distant from S. latifolia (Desfeux et al., 1996;
Mrackova et al., 2008). Some evidence suggests that
the sex-determining system of S. otites, the most
studied species of this group, could be ZW/ZZ
(Correns, 1928; Sansome, 1938). However, work by
Warmke (1942) suggested an XX/XY sex determination system. Genetic mapping performed in a closelyrelated species S. colpophylla (Fig. 2C, D) has shown
that the sex chromosomes of this species evolved from
different pair of autosomes than dioecious species
from the section Elisanthe, and that sex determination in this species is based on male heterogamety
(XX/XY type) (Mrackova et al., 2008). Phylogenetic
analysis proved that the sex chromosomes developed
independently in S. colpophylla and in the species
from the section Elisanthe that are closely related to
S. latifolia (Mrackova et al., 2008). Apart from the
genus Silene, only a few cases of independent origins
of sex chromosomes within one genus have been
reported in plants (Renner & Won, 2001; Renner
et al., 2007). However, extensive phylogenetic studies
analyzing the evolution of dioecy within one genus
have only been performed a few cases (Navajas-Pérez
et al., 2005; Volz & Renner 2008), so it is possible to
expect that more cases of independent origins of sex
determination in related plant species will be found in
the near future.
GENUS RUMEX
The reproductive systems in Rumex are very diverse
and include hermaphroditism, polygamy, gynodioecy,
monoecy, and dioecy (Navajas-Pérez et al., 2005).
In dioecious Rumex species, two different sexchromosomal systems and sex-determining mechanisms have been described: (1) XX/XY with an active Y
chromosome (e.g. Rumex acetosella) and (2) XX/XY1Y2
with sex determination based on the X/A ratio (e.g.
Rumex acetosa) (Navajas-Pérez et al. (2005). There is
one exceptional species Rumex hastatulus, which has
two chromosomal ‘races:’ the Texas race with XX/XY
and the North Carolina race with XX/X Y1Y2. In this
species, the X/A ratio controls sex determination,
although the presence of the Y chromosome is necessary for male fertility (Smith, 1963). In R. acetosa,
repetitive sequence similarity between both Y chromosomes suggests that they probably originated from
one Y chromosome that underwent centromere fission
and gave rise to a pair of metacentric chromosomes
possessing identical chromosomal arms (isochromosomes). These isochromosomes were subsequently
modified by deletions (Rejón et al., 1994). A recent
743
phylogenetic study (Navajas-Pérez et al., 2005) indicates that all dioecious Rumex species evolved from a
common hermaphroditic ancestor. This conclusion suggests that a switch from a sex-determining mechanism
based on the active role of the Y chromosome to a
mechanism based on the X/A ratio occurred during the
evolution of this genus. Such a switch occurred at least
twice independently according to Navajas-Pérez et al.
(2005). The role of the X/A ratio in the sex determination of R. acetosa resembles the sex-determining
system of Drosophila, where the primary genetic sexdetermining signal is provided by the ratio of X-linked
genes to autosomal genes (Pomiankowski et al., 2004).
DIOECIOUS MERCURIALIS ANNUA:
TO M. DOMESTICA?
SIMILARITY
A relatively complex and variable system of sex determination is found in M. annua and its closely related
species. Mercurialis annua is a ruderal species of
pan-European distribution. Three sex-controlling loci
have been described in the dioecious race of M.
annua. The dominant allele at the sex-determining
locus A, together with the dominant allele(s) in at
least one of the other two loci (B1 and/or B2), causes a
male phenotype in the plant. If the recessive allele is
present at the A locus, the plant becomes female
independently of the genotypes at the B1 and B2 loci
(Louis, 1989). It is therefore possible to speculate that
the A locus is the original sex-determining locus and
the B1 and B2 loci are modifiers that developed later.
It is known that plant hormones play an important
role in sex determination in M. annua. Auxins produce
a masculinizing effect on females and cytokinins
produce a feminizing effect on males (independent of
the genotype at B loci; Hamdi, Teller & Louis, 1987).
The plasticity of the sexual phenotype is in apparent
contradiction to the pronounced sexual dimorphism
that is reflected in sex specific gene expression
(Khadka et al., 2005). Sexual dimorphism evolves step
by step as a result of sexually antagonistic selection
(Rice, 1984); therefore, in species where the sex determination was established recently, the level of sexual
dimorphism should be minimal. Studies of M. annua
could therefore contribute to an understanding of the
mechanisms controlling sexual dimorphism and its
evolution. Genes controlling sexual dimorphism
should be linked to the A/a locus. The first steps
towards the isolation of this sex-determining region
have been initiated by Khadka et al. (2005), who
isolated one completely male linked marker. This
system could therefore be interpreted as an XX/XY
sex-determining system with autosomal modifiers
(similar to M. domestica; Dübendorfer et al., 2002).
The importance of M. annua for the evolutionary
studies of sex determination can be illustrated by the
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
744
B. JANOUSEK and M. MRACKOVA
results obtained by Dorken & Pannell (2009). Their
data show that the absence of males in experimental
populations provoked greater male allocation (measured as male reproductive effort; a proportion of the
total above ground biomass allocated to the staminate
flowers). The results obtained in this experiment
support the model for the origin of gynoecium suppressing mechanisms that was proposed by Charlesworth & Charlesworth (1978).
CHANGE IN THE SEX-DETERMINING MECHANISM OF
MERCURIALIS: ANDRODIOECIOUS RACE OF M. ANNUA
Differences in the body plans and life-history strategies can favour higher plasticity of both the genotype
and phenotype in angiosperms compared to animal
models (Kejnovsky, Leitch & Leitch, 2009). Because
the plant body is usually formed by several relatively
independent meristems, the coexistence of branches
with different sexual phenotypes should not lead to
the detrimental effects seen in gonochoristic animal
species (e.g. mammals), where the simultaneous presence of both sexual organs can cause damage in both
sex functions because of hormonal imbalances (Krob,
Braun & Kuhnle, 1994).
Despite this prerequisite, there are just a few
examples of changes in the sex-determining mechanisms in plants. According to Obbard et al. (2006),
androdioecy in hexaploid populations of M. annua may
have evolved as a result of hybridization between
dioecious Mercurialis huetii and monoecious tetraploid
M. annua, an event that brought together the genes for
specialist males with those for hermaphrodites. Interestingly, the results of a study by Pannell (1997)
indicate that male sex in the androdioecious populations is determined by the presence of the dominant
allele of a single sex-determining locus (that suppresses development of female organs) but that males
are prone to sex change in response to environmental
influences (low plant density). It is argued that these
findings help to explain the maintenance of androdioecy in M. annua.
BRYONIA
DIOICA AND DIOECY IN
CUCURBITACEAE
Species of the Cucurbitaceae family are, in contrast to
most angiosperms, characterized by the presence of
unisexual flowers. Of the approximately 800 species in
this family, 460 are monoecious and 340 are dioecious.
Some species produce a mixture of bisexual, female,
and male flowers in various intra- and inter-individual
patterns, and populations can be andromonoecious,
androdioecious, gynomonoecious or gynodioecious
(Kocyan et al., 2007). Phylogenetic studies suggest
that the Cucurbitaceae family has a dioecious origin
(Zhang et al., 2006). Various switches to monoecy or
other types reproductive systems such as androdioecy
occurred frequently during the evolution of Cucurbitaceae, and thus it is difficult to precisely ascertain
how old the sex chromosomes in a given species are
(Renner et al., 2007). The best studied Cucurbitacean
genus containing dioecious species is Bryonia. Genetic
crosses between the dioecious B. dioica and the monoecious Bryonia alba in 1903 provided the first clear
evidence for Mendelian inheritance of sexual phenotypes (dioecy) and made B. dioica the first organism for
which the XY sex-determination was experimentally
proven (Correns, 1907). Applying molecular tools to
this system, Oyama, Volz & Renner (2009) showed
that size of the nonrecombining region differs between
the north-European southern,European populations.
Because of availability of whole genome sequencing
data from the family (see below), the genus Bryonia
could become a good model for the study of the
evolution of sex-determining pathways and sex
chromosomes.
Important data concerning the possible mechanisms
of sex determination in Cucurbitaceae were recently
obtained in melons (Cucumis melo). In this mostly
monoecious species, sex determination is governed by
the genes andromonoecious (a) and gynoecious (g).
Dominant allele of the a locus (CmACS-7 gene;
1-aminocyclopropane-1-carboxylic acid synthase)
causes arrest of the stamen development (Boualem
et al., 2008). The dominant allele of the g locus causes
arrest of the gynoecium development. Monoecious
(A-G-) and andromonoecious (aaG-) plants bear male
flowers on the main stem and, respectively, female or
hermaphrodite flowers on the axillary branches,
whereas gynoecious (AAgg) and hermaphrodite individuals (aagg) only bear female or hermaphrodite
flowers, respectively. The insertion of the Gyno-hAT
transposon in proximity of the g gene (CmWIP1) was
shown to be a cause of the gynoecious phenotype of
several lines (G to g change by hypermethylation of
promoter of the g gene, i.e. CmWIP1). The occasional
presence of the flowers with stamen and reduced
ovaries suggests that the DNA hypermethylations of
the CmWIP1 can be reduced during somatic development of gynoecious plants (Martin et al., 2009). Surprisingly, both CmACS-7 and its homologue from
Cucumis sativa are specifically expressed in female
buds. Role of 1-aminocyclopropane-1-carboxylic acid
synthase in anther arrest appears to be indirect and
inter-organ communication is probably responsible for
the anther arrest (Boualem et al., 2009). The analysis
based on the knowledge of the whole genome sequence
of C. sativa revealed that the evolution of unisexual
flowers in cucurbits may have involved the acquisition
of two ethylene-responsive elements (AWTTCAAA)
and one flower meristem identity gene LEAFYresponsive element (CCAATGT) of the ACS genes.
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
SEX CHROMOSOMES AND SEX DETERMINATION PATHWAY DYNAMICS
Extensive expressed sequence tag analysis in unisexual and bisexual flower buds (using 454 sequencing) revealed that six auxin-related genes (auxin can
regulate sex expression by stimulating ethylene production) and three short-chain dehydrogenase or
reductase genes (homologues to the sex determination
gene ts2 in maize41) are more highly expressed in
unisexual flowers (Huang et al., 2009).
CARICA
PAPAYA
Carica papaya has become an important model for
the studies of sex determination and sex chromosome
evolution because of its relatively small genome and
extremely young sex chromosomes (Liu et al., 2004;
Yu et al., 2008). There are some signs indicating
ongoing degeneration of the areas surrounding the
sex-determining locus in papaya. This pattern,
together with phylogenic data, which indicate a possible dioecious origin of the Caricaceae family, has
lead some researchers to doubt the proposed age of
papaya sex chromosomes (Charlesworth, Charlesworth & Marais, 2005). If the hypothesis of the young
age of papaya chromosomes is accepted, it means
that processes of degeneration in the nonrecombining
region must have worked extremely quickly in this
species. However, recent estimates of the divergence
between the X- and Y-linked genes further support
the young age of the sex chromosomes in C. papaya
(Yu et al., 2008). In addition, specific heterochromatinized DNA-hypermethylated knobs are present in the
nonrecombining region, suggesting a possible role of
epigenetic mechanisms in the sex chromosome evolution (Zhang et al., 2008). The apparent contradiction
of the young age of sex chromosomes and prevailing
dioecy in Caricaceae is proposed by Yu et al. (2008)
to be the product of multiple independent origins of
sex chromosomes in this family. It should be stressed
that an old sex determination system need not be
in a contradiction with the young sex chromosomes.
The possibility that a new sex-determining locus was
recruited, as in the known cases in Oryzias species
(Nanda et al., 2002), cannot be so far excluded. A big
advantage of C. papaya as a model for the future
research is the availability of the draft sequence of its
genome (Ming et al., 2008).
GENUS POPULUS
Genus Populus became an important model object in
the studies of sex determination in the last years.
Primarily, the economic importance of several of its
species promoted genetic mapping studies. The interest of reserchers is mainly focused on the species
Populus trichocarpa as a model tree for whole genome
sequencing studies. A main goal has been to study the
745
genes involved in the synthesis of wood but studies of
the sex determination can profit from the knowledge of
the genomic sequence (Tuskan et al., 2006). Multiple
lines of evidence point to a ZW sex determination
system in Populus, with the female being the heterogametic sex. First, the sequenced tree, Nisqually-1, is
a female, and it showed highly divergent haplotypes in
the sex determination region. Second, suppressed
recombination in this region was only observed in the
female parent of the cross studied by Yin et al. (2008).
Finally, the female heterogamety is also according to
Haldane’s rule (‘When in the F1 offspring of two
different animal races one sex is absent, rare, or
sterile, that sex is the heterozygous [currently =
heterogametic] sex’; Haldane, 1922) in accordance with
the overall male bias in populations of various species
of the genus Populus (Grant & Mitton, 1979; Rottenberg, Nevo & Zohary, 2000).
CONCLUSIONS AND PERSPECTIVES
A comparison of the data for animal models with the
data for plant models that were collected in this review
suggests that the sex-determining pathways in these
two kingdoms evolved by a similarly diverse set
of mechanisms. An overview is provided in the Supporting information (Tables S1, S2). All variants of
the basic sex determination systems found in animal
models were reported also in plants with exception of
the complementary sex determination (haplodiploidy)
that is specific for social insects and aneuploidy-based
sex determination with female heterogamety (ZO/ZZ),
which is found in butterflies. The XX/XO type (also
found in insects) was reported in plants but it has
not yet been sufficiently experimentally supported (in
Dioscorea sinuata; Smith, 1937). The absence of the
total loss of W or Y chromosomes, respectively, can be
explained by an overall younger age of sex chromosomes in plants. Differences between animals and
plants can be found in the form in which plasticity of
sex-determining pathways is manifested. In many
animal species, it is often possible to observe female to
male changes or male to female changes as a result of
environments effects or the manifestation of new sexdetermining genes. In the plant species studied so far,
the cases of sex change to the opposite sex are rare
(Policansky, 1981). The widespread manifestation of
plasticity of sex expression in plants takes the form of
instability of the gynoecium suppression in male
plants (subdioecy). This phenomenon is probably selectively advantageous because it enables species that
have no possibility of active movement to overcome
lack of pollinators and other problems that could
otherwise lead to extinction of strictly dioecious species
(Delph & Wolf, 2005).
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
746
B. JANOUSEK and M. MRACKOVA
The question of somatic sex determination and germline sex determination (often discussed in animal
models) has not yet been studied in plants. Plants
do not set aside a germline in strictu senso. There
is, however, a process enabling plants to limit the
number of necessary cell divisions preceding meiosis.
The cells in the center of the vegetative meristem
possess hypermethylated DNA, and they divide
sparsely. This mechanism lowers the mutation rate
and also reduces the epigenetic influence of environmental factors (Zluvova, Janousek & Vyskot, 2001).
There is therefore at least some similarity to the
germline found in animals.
Another so far neglected question concerns how
a system based on two separate sex controlling
pathways controlled by genes present on the Y chromosome (Charlesworth & Charlesworth, 1978) is
transformed into a system controlled by the pathway
based on the X/A ratio in some species. The following
hypothetical scenario of sex-determining pathway
evolution, based on the observation of the early sex
dimorphism in species with an active Y chromosome,
as well as on the knowledge of the mechanisms
involved in the change of sex linkage in animal
models, can be suggested.
In the first step, dioecy is established in plants
from gynodioecy by the evolution of a gynoecium
suppressing gene in the proximity of the male fertility
controlling gene (Fig. 3A). This process is promoted by
sexually antagonistic selection (Charlesworth & Charlesworth, 1978). The original theory (Charlesworth &
Charlesworth, 1978) assumes just one male sterility
mutation (i.e. that the male fertility locus of gynodioecious ancestor is identical with the anther promoting
gene of the resulting dioecious species). The possibility
of the stepwise shift in the stage of male organ arrest
toward earlier stages was discussed by Zluvova et al.
(2005) but, even if present, this does not influence our
next considerations. The scheme of sex determination
at this stage is outlined in the Supporting information
(Figure S1a). This figure stresses the independence of
the male-promoting and female-suppressing pathways. There are a lack of data concerning the origin
of sex determination in animals. Although there are
indications that sex determination systems of both
insects and vertebrates could have a common origin
(Koopman, 2009), no hypotheses concerning the sex
determination mechanism in their common ancestor
were suggested. A scenario based on two mutations
is also possible in animal models (Charlesworth &
Charlesworth (2005). In this case, the difference
between plants and animals is only in the nomenclature (dioecy versus gonochorism, etc.). In the scheme,
we use universal terms (e.g. male organ promoter
instead of anther promoter) to stress that this processes can occur not only in plants.
In the second step, sexually antagonistic selection
continues and improves the linkage of the sexdetermining loci. Sex chromosomes that are created by
this process can continue to accumulate sexually
antagonistic alleles (Rice, 1984) (Fig. 3B). Even in
species that are at this stage of sex determination, it is
possible to find early expressed sexual dimorphism
(e.g. S. latifolia; Zluvova et al., 2008b; J. Zluvova
unpublished data).
In the third step, the sex-determining genes start
to accommodate to the sex specific gene expression
patterns controlled by the sexually antagonistic
gene(s) and their expression starts to be controlled by
these genes. Eventually, the gene(s) that were previously controlling only sexual dimorphism become(s) a
sex-determining gene(s). For reasons of space,
Figure 3C shows the situation in males only. The
situation in females is shown in the Supporting information (Fig. S1). It is known that sexually antagonistic genes are evolving fast (Qvarnström & Bailey,
2009). A good example of the fast evolution of
Y-linked genes in plants was revealed in S. latifolia,
where a lack of the Y chromosome can not be completely compensated for by the presence of the
genome of the related species Siline viscosa, and
anther defects in the hybrid between S. latifolia and
S. viscosa resemble two different mutants lacking
part of Y chromosome (Zluvova et al., 2005). The
active role of the Y chromosome in sex determination
is still preserved because the new sex-determining
locus is still located on the Y chromosome. The
important difference from the previous stages is that
connection between the control of the stamen promotion and anther suppression is established. This
opens new possibilities for the evolution of the sexdetermining system.
In the fourth step, two alternative scenarios are
possible. The original sex-determining loci can be
lost from the Y chromosome just by chance or, more
parsimoniously, the translocation of the original sexdetermining region to the autosomes could be supported by Y chromosome degeneration as a result of the
absence of recombination (Fig. 3D). Because male
organ promotion and female organ suppression are
already controlled by the single controlling pathway,
the genotypes possessing translocation of these genes
to autosomes can be selected for because they can
escape from the process of degeneration. The change
of the position of these genes does not influence
the sexual phenotype because the genes show sexlimited expression, and they are controlled by the gene
derived from the gene originally controlling only
sexual dimorphism).
In the fifth step, the secondary sex-determining
locus loses its controlling role as well, and control
of sex determination is coopted by alternative
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
SEX CHROMOSOMES AND SEX DETERMINATION PATHWAY DYNAMICS
747
A
female organ suppressor
male organ promoter
male organ
promoter
female
hermaphrodite
gynodioecy
female
male
dioecy
B
SAG-F
SAG-M
female organ suppressor
female organ suppressor
male organ promoter
proto-X
proto-Y
C
male organ promoter
X
female organ
suppressor:
present
Y
Early expressed
SAG-M present
male organ
promoter:
present
Male specific expression profiles
female organ
absent
male organ
present
Male specific expression
profiles
female organ
suppressor:
on
female organ absent
D
SAG-F
SAG-M
female organ suppressor
male organ promoter
autosomes X Y
E
SAG-F
male organ present
SAG-F
female organ
suppressor.
male organ promoter
autosomes
SAG-M
(sex
determining)
X Y
SAG-F
SAG-M
(sex determining)
SAG-M
autosomes X Y
male organ
promoter:
on
SAG-M
autosomes
X Y
Figure 3. The evolution of the sex-determining pathways in plants. A, theory of origin of dioecy via male sterility
suggested by Charlesworth & Charlesworth (1978). Both the female organ (gynoecium) suppressor and the male organ
(anther) promoter promoter act independently but their coordination is achieved by their close location on the
Y-chromosome or by their location in the nonrecombining region of the Y-chromosome. B, formation of sex chromosomes.
Accumulation of sexually antagonistic genes and reduction of recombination frequency between female organ (gynoecium)
suppressor and male fertility controlling genes creates sex chromosomes. For simplification, only one sexually antagonistic
gene (SAG) is presented. SAG-F means sexually antagonistic alelle advantageous for females and SAG-M means
male advantageous sexually antagonictic allele of the same gene. C, sexually antagonistic gene(s) based switch in the
sex-determining pathway. Sexual dimorphism (i.e. controlled by SAG-M) is improved step by step and starts to act before
the Y-linked genes involved in female and male organ development control. At certain stage, the expression of both the
female organ suppressor and the male organ promoter becomes sex-limited as a consequence of their adaptation to sex
specific expression profiles of other genes. D, restructuration of sex chromosomes. Female organ suppressor and male
organ promoting gene(s) are lost from the Y chromosome and transferred to autosome(s). E, origin of the X/A based
sex-determining system. SAG-M is lost from Y-chromosome and transferred to an autosome. The X/A ratio becomes crutial
for sex determination because SAG-M pushes development toward the male direction in contrast to SAG-F that pushes
development toward female direction.
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 737–752
748
B. JANOUSEK and M. MRACKOVA
mechanisms such as an X/A ratio-based mechanism
(Fig. 3E). The switch could be based on the mechanisms described in fishes and insects, in which one of
the genes, ‘a slave’ in the sex-determining pathway
located on the X chromosome, can become ‘a master’.
Simultaneously, the function of this new master gene
is influenced by the genes located on autosomes. An
important prerequisite of this kind of transformation
of sex-determining system is that male organ promotion and female organ suppression are controlled by
the same pathway.
Veltsos et al. (2008) described processes that may
influence the spread of new sex-determining mechanisms. In this case, the invasion of the degenerated Y
chromosome (in the hybrid zone) can cause selection
in favour of the new type of X chromosome that is
able, in combination with autosomal loci, to determine sex in a given species. It is apparent that, in
most plant species and in many animal species, this
evolution is not complete because many species still
rely on an active role of the Y chromosome in sex
determination.
Instability of sex expression and/or cytologically
homomorphic sex chromosomes are sometimes taken
as a sign of the primitive status of the evolution of
sex-determining systems in some plant species
(Vyskot & Hobza, 2004). Data obtained in the animal
models suggest that even very advanced sexdetermining systems (as in mammals) can show a
considerable plasticity of sex expression (Bianchi,
2002); thus, the sequencing of the sex-determining
regions of the studied species should be the method of
choice used to ascertain the age of sex chromosomal
systems. Additionally, a more detailed phylogenetic
approach should answer the question of the age of
sex-determining pathways in model dioecious species.
Studies of mechanisms at the molecular level should
not be limited to the single chosen models from the
studied families. As can be deduced from the data
obtained in animal models, the comparative analysis
connecting the detailed study of sex-determining
regions with detailed phylogenetic approaches is the
best way to aim for an understanding of the regularities (and irregularities) in the evolution of sex determination and sex chromosomes.
ACKNOWLEDGEMENTS
This work was supported by the Grant Agency of
the Academy of Sciences of the Czech Republic
(IAA600040801 to B.J.), by the Czech Ministry of
Education (LC06004), and by the Academy of Sciences
of the Czech Republic, grants no. AV0Z50040507 and
AV0Z50040702.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Figure S1. Sexually antagonistic gene(s) based switch in the sex-determining pathway changes in females:
changes in females.
Table S1. Overview of mentioned fungal and animal species.
Table S2. Overview of the mentioned plant species.
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