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Plant Physiol, December 2001, Vol. 127, pp. 1418-1424
SCIENTIFIC CORRESPONDENCE
Dioecious Plants. A Key to the Early Events of Sex Chromosome
Evolution1
 oan
Negrutiu,*
Boris
Vyskot,
Nicolae
Barbacar,
Sevdalin
Georgiev, and
Francoise
Moneger
Reproduction and Developmental Biology, Ecole Normale Superieure de
Lyon, 46 Allée d'Italie, 69364 Lyon cedex 07, France (I.N.,
N.B., S.G., F.M.); and Institute of Biophysics, Czech Academy of
Sciences, Kralovopolska 135, 612 65 Brno, Czech Republic (B.V.)
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INTRODUCTION |
Around 200 BC, the Nordic
tribes devised rune symbols to represent the forces of nature. Among
these symbols were X-GEBA, the rune of love and sexuality, and
Y-FEOH, the rune of success. It was believed that by picking the right
rune, the wearer could harness the power the rune represented. Hazard
or deep intuition? It turns out that in biology, X and Y symbols define
sexual fates and reproduction success.
Sex determination systems based on heteromorphic X and Y sex
chromosomes are particularly interesting to study from both a developmental and an evolutionary perspective. There are many parallels
between the sex determination systems, as well as the organization of
sex chromosomes, in different species, even between animals and plants.
Two main systems of chromosomal sex determination, XY and X:A
(autosomal chromosome) ratio, apparently have evolved many
times. Mammals, for example, have the XY system, with a dominant
(active) Y chromosome containing the key sex determination function(s), whereas Drosophila melanogaster has an X:A system, where the
ratio of X:A chromosomes determines sex by an X chromosome counting system, the Y chromosome being largely dispensable (Hodgkin,
1992 ).
Dioecy is a widespread condition in flowering plants, despite their
recent evolutionary origin: 6% of the 240,000 angiosperm species are
dioecious and 7% of 13,000 genera of angiosperms include dioecious
species, suggesting that it has arisen many times during flowering
plant evolution (Renner and Ricklefs, 1995). Dioecy is correlated with
perennial climbing growth, wind, or water pollination and has a
preponderance in tropical flora. Model species with a chromosomal sex
determination are white campion (Silene latifolia; XY
system), hop (Humulus lupulus; X:A
system), and sorrel species (Rumex spp.) which include both XY-like and X:A systems
(Figs. 1 and 2).
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Figure 1.
Historical pictures of meiotic preparations
showing terminal pairing of X and Y chromosomes in male flowers of: a,
white campion (2n = 24, XY, metaphase I; van
Nigtevecht, 1966); b, hop (2n = 20, XY, early anaphase
I, arrows; Moutchen et al., 1973); and c, sorrel (Rumex
acetosa; 2n = 15, XY1Y2, metaphase I, with
sex-trivalent XY1Y2 in convergent orientation; Parker and
Clark, 1991).
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Figure 2.
Root tip metaphases of dioecious sorrel female (a)
and male (b). Metaphases from permanent hairy root cultures of
dioecious white campion female (c) and male (d), and related
gynodioecious Silene vulgaris (e) and hermaphrodite
Silene chalcedonica (f). Sex chromosomes are
indicated. Bar = 10 microns.
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Plant sex determination has been recently and extensively covered
(Ainsworth et al., 1998); therefore, we will mainly concentrate on the
contribution of this very particular group of plants to the universal
question of sex chromosome evolution.
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A SURPRISING DIVERSITY OF SEX DETERMINATION MECHANISMS |
In animals, sex determination processes usually involve a similar
basic strategy: a primary (genetic) signal, a master regulator that
responds to the signal, and a double-switch gene selecting between two
alternative sexual programs (Nöthiger and Steinmann-Zwicky, 1987). The molecular mechanisms vary extensively, and can differ within
genera or even within a species. For example, Sxl, the master regulatory gene in certain Drosophila spp., is
present in other flies, all of which have separate sexes and sexual
dimorphism, but Sxl does not appear to control sex
determination in the latter (Wray and Abouheif, 1998).
The corresponding mechanisms have not been characterized at the
molecular level in dioecious plants so far, but it is clear that sexual
dimorphism is a late developmental decision during the life cycle of
the plant, mainly restricted to flower organogenesis or reproductive
organ differentiation. It is interesting that in plant species with
clearly identified sex chromosomes such as hop, sorrel, or white
campion (Fig. 1), the sexual dimorphism is expressed at very early
stages of flower development, namely at stages of organ initiation or
specification (Farbos et al., 1997; Ainsworth et al., 1998). In other
words, sex determination processes in these species act in a male or
female whorl-specific manner at or just downstream but independent of
the ABC flower regulatory network (Ainsworth et al., 1998, and
refs. therein; Scutt et al., 1999). Therefore, understanding flower
development in model species such as Arabidopsis is essential in
addressing the question of how sex determination might work in
unisexual plants.
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X AND Y SEX CHROMOSOMES: ALWAYS THE SAME TUNE? |
The evolution of heteromorphic sex chromosome systems in widely
differing species suggests that similar forces have been at work in
every case. The outcome is the accumulation on the sex chromosomes of
key genetic components (molecular switches) determining sexual
dimorphism and, following a controlled arrest of recombination along
most regions of X and Y, the concentration of sex-related genes on sex
chromosomes, Y chromosome genetic isolation and erosion, X chromosome
dosage compensation, etc. (Charlesworth, 1992; Ellis, 1998;
Charlesworth and Guttman, 1999; Mitchell, 2000).
Taken together, the above can be summarized as follows: (a) Sex
determination exhibits similarities (such as male heterogamety, extensive sexual dimorphism, and X chromosome dosage compensation) that
have arisen by convergent evolution. Sex determination is probably the
most typical case where evolution can produce a variety of solutions to
the same basic problems in development (Hodgkin, 1992); and (b) Plants
are key players in the study of the evolution of sex determination
because they offer a unique opportunity in giving access to the very
early stages of X and Y chromosome history.
Because this is a critical matter in developmental and evolutionary
biology, we have chosen to illustrate this latter point by using sorrel
and white campion as examples in the more general context of sex
determination. Sorrel will be briefly introduced, whereas a more
detailed analysis of white campion is envisaged in regard to the
similarities of this plant and mammalian XY system (Westergaard, 1958;
van Nigtevecht, 1966; Ciupercescu et al., 1990).
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SORREL: A "MULTIPLE" SEX DETERMINATION SYSTEM |
Sorrel (Fig. 2, a and b) has a multiple sex chromosome system with
two X chromosomes in females (2n = 14, XX) and one X
plus two Y chromosomes in males (2n = 15, XY1Y2). In this species, sex determination is controlled by activities of genes located both on
the X chromosome and on the autosomes (Ainsworth et al., 1998). The
male flower phenotype is not dependent on the presence of the Y
chromosomes, but they are necessary for the production of fertile
pollen. The two Y chromosomes are highly heterochromatic, which can be
demonstrated by simple staining. Recent studies have revealed that the
Y chromosomes have accumulated numerous repetitive DNA sequences, with
at least one family being unique to the Y (Shibata et al., 1999). The Y
chromosomes maintain their condensed status also in interphase, thus
forming two peripheral bodies in male nuclei. Immunostaining
experiments demonstrated that the Y bodies display a characteristic
epigenetic modification: depletion of H4 histone acetylation (Lengerova
and Vyskot, 2001). Thus, the sorrel Y chromosomes represent an example
of constitutive heterochromatin, which is not true of the white campion
Y chromosome (Grant et al., 1994; Scutt et al., 1997). From this
difference, we infer that the sex chromosomes of sorrel are older than
those of white campion.
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THE GENUS SILENE: A BOTANIST'S POINT OF
CONTENTION |
White campion (previously Melandrium album), belongs to
the genus Silene. The genus contains more than 700 species
in 44 sections, and possesses a range of reproduction modes, from
hermaphroditism through gynodioecy and occasional monoecy to stable
dioecy (Chater and Walters, 1964; Desfeux and Lejeune, 1996). It now
includes the previously separate genera Melandrium and
Lychnis. Even though their chromosome number is the same
(2n = 24; Fig. 2, c-f; Degraeve, 1980), there
is high heterogeneity in genome size, indicating an accumulation of
numerous DNA repeats in some species (Siroky et al., 2001). For
example, flow cytometric analysis revealed a small genome size in
gynodioecious S. vulgaris (section Inflatae, 2.25 pg of DNA
per diploid nucleus [pg/2C]) and Silene
pendula (section Erectorefractae, 2.35 pg/2C), but large values in
dioecious white campion (section Elisanthe, 5.73 pg/2C) and
hermaphrodite S. chalcedonica (previously Lychnis
chalcedonica, section Lychnidiformes, 6.59 pg/2C). Moreover, a
great variation in number and localization of rDNA loci (two - seven
nuclear organizing regions) was found among these species
(Siroky et al., 2001). All these data clearly demonstrate that nuclear
genomes of Silene spp. are highly diversified.
Recently constructed molecular phylogenies based on rDNA intergenic
spacer sequences suggest that in the last 20 to 25 million years, separate sexes evolved at least twice within the genus (the
white campion versus Silene otites branches), in
agreement with more classical classification criteria (Degraeve,
1980; Desfeux and Lejeune, 1996). However, the form of
sex determination in different sections of the genus remains
controversial and the support for some branches in the intergenic
spacer sequences clustering is weak. Additional comparative sequence
data are required to improve the resolution of phylogenetic
relationships between key dioecious (white campion and S. otites) and hermaphrodite species (Silene conica
and Silene gallica), as well as to estimate the age of the
sex chromosomes across the tree by evaluating the time since
recombination between defined X and Y loci or regions has ceased (see below).
These are critical questions to be answered if we want to understand
why, among the many dioecious species, only a few have evolved sex
chromosomes, a handful of which possess an XY sex determination system
(Charlesworth and Guttman, 1999). The fact that the genus
Silene contains species that evolved X and Y chromosomes makes it an attractive system in the study of breeding system evolution
in general and sex chromosome evolution in particular.
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THE XY SEX CHROMOSOME SYSTEM |
The two sexes share a common gene pool while performing many
different biological functions. In the case of mammals and white campion, the presence or absence of the Y determines which reproductive organs, male or female, will develop. Thus, the Y is dominant and
active with regard to sex determination.
From Genic to Chromosomal Systems of Sex Determination
All sex chromosomes are believed to be derived from pairs of
autosomes. Proto-X and -Y chromosomes are considered to contain a
simple diallelic system of sex determination. The case of the SUPERMAN (SUP) gene, which, when mutated, causes
imperfect unisexuality in Arabidopsis, could illustrate how primitive
genic sex determination systems might arise. Although certain
sup alleles (sup-1) enhance maleness in agreement
with the gene name, others, including epialleles exhibiting gene
hypermethylation (clk alleles; Jacobsen and Meyerowitz, 1997; Rohde et al., 1999, and refs. therein), produce a rather distinct
"super-woman" phenotype. The result is a contrasting series of SUPm
(male enhancing) and a SUPf (female enhancing) states (Fig.
3a). Such states need to be subsequently
enforced by the action of other, genetically linked, sexually
antagonistic genes and modifier genes differentially acting on such
alleles (Charlesworth, 1992; Rice, 1992).
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Figure 3.
Epigenetic control of flower development. DNA
methylation changes often lead to modification in floral patterns. a,
Hypermethylation of the SUPERMAN gene displays an increase
in number of anthers and/or carpels in Arabidopsis (Jacobsen and
Meyerowitz, 1997). b, Epigenetic inactivation of a CYCLOIDEA
homolog is responsible for variation in floral symmetry in
Linaria vulgaris (Cubas et al., 1999). c, A global
CpG hypomethylation of nuclear genome of white campion by
5-azacytidine induces a sex reversal from male to androhermaphrodite
phenotype. This epimutation was likely located on the Y chromosome
because it displayed holandric inheritance and the genes controlling
carpel suppression are Y linked (Janousek et al., 1996). 5-Azacytidine
is expected to activate genes, whereas in this case an inactivation of
female suppressor genes located on the Y chromosome was observed. One
plausible explanation is that a large and global CpG
hypomethylation induced by 5-azacytidine could disturb nDNA methylation
patterns in such a way that some gene regions were (CpNpG)
hypermethylated and thus inactivated, as demonstrated at the
Arabidopsis SUP locus (Jacobsen et al., 2000; Lindroth
et al., 2001).
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The situation in white campion and other dioecious species
with established sex chromosome systems indicates that more than one
locus is involved in sex determination, as shown by both crosses between dioecious plants and related monoecious or hermaphrodite species (reviewed by Westergaard, 1958), or by mutagenesis (Lardon et
al., 1999 a, 1999b). In white campion, sex determination is controlled by at least three loci (Lardon et al., 1999b). The Y
chromosome contains two of these loci: a female suppression function,
negatively controlling cell proliferation during carpel initiation, and
a male promoting function controlling the specification of male
gametophytic cell fate. That these are independent pathways for male
and female developmental arrest is reflected by the fact that changes
in sex expression generate either hermaphrodite or asexual (neuter,
both male and female sterile) mutants. The genetic analysis of gamma
ray-induced mutants has enabled us to distinguish two loci with female
suppression properties: a Y-linked locus (called GSF-Y) and
an autosomal locus (called GSF-A). In this context,
GSF-A appeared as a potential enhancer of the
GSF-Y locus. Phenocopies of such mutations were induced
chemically when genetically male plants were treated with
5-azacytidine, a DNA demethylation agent (Fig. 3c), or trichostatin A,
a potent inhibitor of histone deacetylases (Janousek et
al., 1996; J. Hodurkova and B. Vyskot, unpublished data). We conclude
that sex expression control in white campion can be added to the list
of flower developmental processes that are regulated epigenetically
(Finnegan et al., 2000; Jacobsen et al., 2000; Fig. 3).
What is the nature of evolutionary processes that
turn proto-X and -Y chromosomes into heteromorphic sex chromosomes? Key events appear to be the suppression of meiotic recombination
between protosex chromosome regions in the heterogametic sex, Y
degeneration, and X chromosome dosage compensation (Charlesworth, 1992;
Ellis, 1998).
Arrest of X-Y Recombination: A Critical Event in the Evolution of
Sex Chromosomes
The reduction and subsequent suppression of recombination between
the sex determination loci and the male-advantage/female-disadvantage genes linked to them is most likely selected for to avoid production of
neuters or hermaphrodites (Rice, 1987; Charlesworth and Guttman, 1999).
From this point onwards, the differentiation of sex chromosomes can
begin, with an increasing functional differentiation between the
initial homologs resulting in morphologically and genetically distinct
sex chromosomes. Sex chromosome differentiation appears to be a
continuing process.
The mechanism that underlies the lack of recombination between sex
chromosomes in males may be of great importance in the evolution of the
Y chromosome because it could determine the nature and timing of
subsequent genetic events. Recombination can be suppressed by: (a)
chromosomal inversions, or (b) more specific control functions
restricting the pairing of defined pairs of chromosomes (recombination
modifiers; Nei, 1969; also see Charlesworth and Charlesworth, 1980).
Models proposed by these authors predict that recombination suppression
can occur with sex-specific selection.
The strata model in the human XY system is illustrating the first cited
mechanism. Lahn and Page (1999) have proposed a model in which human Y
chromosome evolution involved four inversion events, each suppressing
X-Y recombination separately and without disturbing gene order on the
X. These events spanned along a time scale of 240 to 300 million years
of animal evolution. The results show that in humans, the arrest of XY
recombination has occurred progressively. In Drosophila
spp., on the contrary, the breakdown of recombination has apparently
taken place quite suddenly (Clark, 1988), and might correspond
to the second mechanism.
These situations need to be evaluated experimentally in
Silene spp. by looking, on the one hand, for the existence
of strata and, on the other hand, for sterile mutants defective in
meiotic pairing. In the first case, for example, a molecular
characterization of sex-linked loci is required. The first active
Y-linked genes described have a very similar X chromosomal copy and the
relative age of individual X-Y gene pairs has been measured by
nucleotide divergence (Delichère et al., 1999; Filatov et al.,
2000; Atanassov et al., 2001). The results indicate, as for
human XY-linked genes, that the two loci characterized so far identify
Y chromosome regions that have ceased recombining at different times
during the evolution of sex chromosomes, namely 5 and 15 million years
on the 20- to 25-million year scale since the last common hermaphrodite
ancestor. They reveal distinct events in the evolutionary history of
the sex chromosomes and stimulate further studies in this direction.
Y Organization Indicates Functional Coherence
Recombination suppression and concomitant evolution of dosage
compensation are believed to be necessary to avoid exchanging the
accumulating dysfunctional genes from the Y onto the X (Clark, 1988).
Because there is only one Y for four autosomes and three X chromosomes
in a population, the Y is much more sensitive to genetic drift (random
fluctuations of gene frequencies; Nei, 1970). Events such as sequence
translocations, insertions, inversions, or amplification, associated or
not with (retro) transposition are documented in the human Y chromosome
(Schwartz et al., 1998, and refs. therein). Therefore, the evolution of
the Y chromosome reflects these basic properties. Contrary to ordinary
chromosomes containing random assortments of genes, the gene content in
the large non-recombining Y region of the human Y appears as a
functionally coherent exception (Lahn and Page 1997), in that there is
tendency to accumulate male-benefit genes by selectively retaining and amplifying male fertility factors or genes that enhance male
reproduction fitness. These are linked to the sex determination loci.
In other words, the Y becomes an increasingly specialized male
chromosome and this specialization parallels the deterioration of the
genetic content of the large non-recombining Y region (Mitchell,
2000).
The gene content of the Y chromosome of white campion shows that 15 to
20 million years of XY evolution is sufficient to achieve a
"functional coherence" of Y chromosome organization: In addition to
the genes involved in sex determination (see above) and sex ratio bias
that localize on the p arm (Lardon et al., 1999b), the Y chromosome
carries several loci involved in stamen differentiation and
microsporogenesis (Donnison et al., 1996; J. Zluvova and S. Georgiev,
unpublished data) that are concentrated on the q arm, together with
several of the cloned Y-linked genes that have X homologs (see also
Fig. 4). The working hypothesis is that
the p arm contains the block of sex determination genes and is rather gene poor, whereas the q arm concentrates several male-specific functions and contains regions of homology with the X.
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Figure 4.
Immortal hairy root cultures of white campion
serve as a permanent source of synchronized metaphases. Due to their
large size, the sex chromosomes are a suitable material for laser flow
sorting. Because the X chromosome is nearly twice as large as compared
with the average autosome, it can easily be purified and used for
physical localization of genes by PCR and construction of
chromosome-specific libraries (Kejnovsky et al., 2001). The purity of
the sorted X and autosomes is high (95%) as estimated by both
fluorescence in situ hybridization and PCR reconstruction
experiments. The physical mapping is illustrated by the autosomal
localization of MROS4, the autosomal and X location of
MROS3 (Matsunaga et al., 1996), and the unique position of
SlX4 on the X chromosome (Atanassov et al., 2001).
0, Control, no DNA template; A, autosomes; X, X chromosomes; m, male
genomic DNA; f, female genomic DNA; M, marker
(pBR322/AluI).
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Evidence for Y Decay and X Chromosome Dosage Compensation in
Silene Spp. Remains Ambiguous
At present, experimental evidence for X chromosome inactivation
based on methylation and H4 acetylation patterns in white campion
female cells remains ambiguous (Vyskot et al., 1993; Siroky et al.,
1999). Furthermore, evidence for Y degeneration in white campion is
relatively weak. It is based on YY seedling lethality (Westergaard,
1958), on the large size of the Y relative to the X or autosomes in
several related hermaphrodite species suggesting that the Y has been
accumulating DNA (Figs. 2 and 4), and on the identification of the
first X-linked gene shown to have a degenerated counterpart on the Y
(Guttman and Charlesworth, 1998). On the other hand, the sex
chromosomes in white campion were reported to have the same length as
the longest autosomal pair in certain non-dioecious Silene
spp. belonging to the Lychnidiformes section (Degraeve,
1980), there is important repetitive sequence similarity between
the sex chromosomes and autosomes of white campion (Scutt et al.,
1997), and the Y chromosome is largely non-heterochromatic with all
Silene spp. chromosomes, Y included, possessing strikingly gene-dense regions near their ends (as shown by early DNA-replicating patterns and fluorescence in situ hybridization signal profiles following hybridization with a total cDNA library; Vyskot et al., 1999).
At the population genetics level, a reduction in the effective
population size of Y-linked genes is observed when estimating sequence
divergence at non-synonymous and silent sites in pairs of active genes
on the sex chromosomes, showing that some selective processes do affect
this plant Y chromosome (Filatov et al., 2000). Further work on
additional loci is needed to evaluate more precisely which genetic
processes contribute most to coding sequence evolution on sex
chromosomes and to the genetic erosion of Y-linked alleles (Charlesworth and Charlesworth, 2000). Taken together, evidence is
accumulating in support of a recent origin for the XY chromosome system
within the genus Silene.
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CONCLUSIONS: THE MANY REASONS TO SUPPORT RESEARCH ON PLANT SEX
CHROMOSOME SYSTEMS |
Male genomes consist of an association of three nuclear
subgenomes: the autosomes, the X and the Y. Each component, although living under the same roof, has distinct evolutionary constraints and
fates. In this respect, the Silene genus is an example of how the evolution of an XY system contributes to morphological change
and speciation.
The Y chromosome differs from all other chromosomes not only in that it
is the only chromosome that does not recombine along the majority of
its length, but also in being present only in the male sex in a
permanent haploid condition (Y genetic isolation), in having a common
ancestry and persistent meiotic relationship with the X, and the
tendency of its genes to degenerate during evolution (Y genetic
erosion). The Y becomes a specialized male chromosome, which
essentially behaves like a single recombination unit. The lesson we can
learn from white campion in this context is that a functional coherence
of the Y can be achieved relatively early during Y evolution, which
might be an essential condition for the maintenance of an XY system.
Concerning Y decay and X chromosome dosage compensation, there is so
far no solid evidence that either of these two stages has been reached.
Therefore, we anticipate that white campion will help to elucidate the
evolutionary forces that shape the genetic content of a Y chromosome
during the early stages of its evolution. Sex chromosomes in animals go
back 300 million years and Y chromosomes are genetically eroded (Ellis,
1998; Mitchell, 2000). Because similar constraints operate in all sex
chromosome systems, the Silene genus with its estimated 20- to 25-million year ancestry appears to contain the most recently
evolved XY system known so far in Eukaryotes, therefore holding the key
to at least one major question: How did all this start?
In brief, in white campion, the first active genes on the Y have been
identified, a large collection of Y deletion mutants is available, and
a powerful chromosome technology is being established (Fig. 4). Such
tools can be transposed to other species within the Silene
genus. We now have the opportunity to perform a comparative analysis
with chosen members of the Silene genus that do not have heteromorphic sex chromosomes to characterize in depth such early evolutionary stages, to test different hypotheses, and hopefully to
clone the sex determination master genes of white campion in the (near) future.
More generally, dioecious plants with XY sex determination systems are
typical flowering plants with a modular and sequential developmental
strategy and, at the same time, resemble animals in their sexual
reproduction strategy. Therefore, the full understanding of the
evolution of sex chromosomes can only be achieved by integrating the
molecular aspects of sex determination from dioecious plants.
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ACKNOWLEDGMENTS |
The authors are grateful to Charlie Scutt and John Bowman for
the critical reading of the manuscript and to the reviewers for very
helpful and constructive comments.
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FOOTNOTES |
Received August 10, 2001; returned for revision August 27, 2001; accepted September 17, 2001.
1
This work was supported by the Grant Agency of
the Czech Republic (grant nos. 521/99/0696 and 521/96/K117 to B.V.) and
by Action Concertée Incitative (grant no. MRT/52b to F.M.
and I.N.).
*
Corresponding author; e-mail Ioan.Negrutiu{at}ens-lyon.fr; fax
04-72-72-86-00.
www.plantphysiol.org/cgi/doi/10.1104/pp.010711.
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INTRODUCTION
A SURPRISING DIVERSITY OF...