The Evolution of Sex Chromosomes and Dosage
Compensation in Plants
Aline Muyle*, Rylan Shearn, and Gabriel AB Marais
Laboratoire de Biome
´
trie et Biologie Evolutive (UMR 5558), CNRS/Universite
´
Lyon 1, Villeurbanne, France
*Corresponding author: E-mail: aline.muyle@univ-lyon1.fr.
Accepted: February 13, 2017
Abstract
Plant sex chromosomes can be vastly different from those of the few historical animal model organisms from which most of
our u nderstanding of sex chromosome evolution is derived. Recently, we have seen several advancements from studies on
green algae, brown algae, and land plants that are providing a broader u nderstanding of the variable ways in which sex
chromosomes can evolve in distant eukaryotic groups. Plant sex-determining genes are being identified and, as expected,
are completely different from those in animals. Species with varying levels of differentiation between the X and Y hav e been
found in plants, and these are hypothesized to be representing different stages of sex chromosome ev olution. However, we
are also finding that sex chromosomes can remain morphologically unchanged over extended periods of time. Where
degeneration of the Y occurs, it appears t o proceed similarly in plants and animals. Dosage compensation (a phenomenon
that compensates for the consequent loss of expression from the Y) has now been documented in a plant system, its
mechanism, however , remains unknown. Research has also begun on the role of sex chromosomes in sexual conflict
resolution, and it appears t hat sex-biased genes evolve similarly in plants and animals, although the functions of these
genes remain poorly studied. Because the difficulty in obtaining sex chromosome sequences is increasingly being overcome
by methodological developments, there is great potential for further discovery within the field of plant sex chromosome
evolution.
Key words: Y degeneration, dioecy, sex chromosome turnover, sex-biased expression, sex chromosome sequencing.
Introduction
Sex chromosomes are unique in that each member of the
chromosome pair has genetic material that differs partially
from the other, giving a mechanism by which the sex of indi-
viduals can be determined. There are three systems by which
this happens (
fig. 1). One is the female heterogametic system,
where females have two distinct sex chromosomes (ZW) and
males are homogametic (ZZ), as can be observed in some
willows, for example Salix suchowensis (
Hou et al. 2015).
Another is the male heterogametic system, such as that
found in Silene latifolia (Bernasco ni et al. 2009), where
males have two distinct sex chromosomes (XY) and females
are homo gametic (XX). In species with an independent hap-
loid phase in their life cycle, sex can be determined in the
haploid gametophytes by a UV system (females U, males V)
and the diploid sporophyte is then heterogametic (UV), as
observed for example in Marchantia polymorpha (
Yamato
et al. 2007).
Sequence comparison within and between species of well-
studied animal models suggests that sex chromosomes derive
from an ordinary pair of autosomes that have evolved sex-
determining genes and stopped recombining (
Bachtrog
2013
). For example, in placental mammals, Drosophila,and
birds, most of the Y (or W) chromosome has stopped recom-
bining (
Bachtrog 2013; Ellegren 2011). As a result, this non-
recombining region degrades; the human Y chromosome, for
example, has lost most of its original genes (
Ross et al. 2005).
The resulting imbalance of X genes (one copy of X genes in
males vs. two in females) appears to have been countered by
the evolution of dosage compensation in some animals, a
mechanism that theoretically enables equivalent X gene ex-
pression in both sexes (
Graves 2016).
Most of this knowledge on sex chromosome evolution
comes from a few animal models, but a broader phylogenetic
perspective is essential to test whether it can be generalized to
other eukaryotes. Outside animals, sex chromosomes have
mainlybeenstudiedinlandplants,andtoalesserextentin
GBE
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green and brown algae. Consequently, this review will mainly
focus on plant sex chromosomes and will mention data on
algae whenever available.
Specifically, this review will cover the recent advances from
studies on nonanimal systems that are giving us a more global
perspective on the range of ways in which sex chromosomes
evolve. It will explore the particularities of plant sex chromo-
somes regarding their origins and sex-determining genes, and
discuss what they teach us about the causes of recombination
suppression and the consequent degeneration of sex chromo-
somes. What follows is a presentation of why in some species,
recombination suppression does not spread outside of the
FIG.1.—Examples of sex chromosome systems in plants. (a) XY: male heterogamety (Silene latifolia), (b) ZW: female heterogamety (Salix suchowensis)
and (c) UV: haplo-diploid system (Marchantia polymorpha), showing maternal (pink) and paternal (blue) sex chromosomes.
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small region containing the sex-determining genes. The fields
of plant dosage compensation and sexual conflict resolution
are also explored, two topics that have not yet been tackled by
recent reviews on plant sex chromosome evolution
(
Charlesworth 2016, 2015; Vyskot and Hobza 2015). Finally,
with methodological advances making it easier than ever to
obtain sex chromosome sequence data, there is great poten-
tial for new findings in this field, and suggestions for future
research directions are provided.
The Origin of Sex-Determining Genes and Sex
Chromosomes in Plants
Very few (~40) sex chromosomes have so far been identified
in plants (
Ming et al. 2011). This contrasts dramatically with
the number of dioecious plants (species with male and female
individuals, i.e., species that are likely to carry sex chromo-
somes). Indeed, 75% of liverworts (6,000 species), 50% of
leafy mosses (7,250 species), 36% of gymnosperms (381 spe-
cies), and 5–6% of angiosperms (15,600 species) are dioe-
cious (
Ming et al. 2011; Renner 2014). Estimates of the
frequency of dioecy in brown and green algae are currently
missing. In angiosperms, hermaphroditism is supposedly the
ancestral breeding system (
Endress and Doyle 2015; Sauquet,
seminar communication), and some families are entirely dioe-
cious (
Kaferetal.2014; Renner 2016) such as Salicaceae
(
Manchester et al. 2006), Caricaceae (Carvalho and Renner
2012
), and Ebenacaeae (Akagi et al. 2014), which suggests
that dioecy is ancient in these families. However, dioecious
and hermaphroditic species are often assigned to the same
angiosperm genus, which suggests that dioecy is often of
recent origin. Homomorphic sex chromosomes (where both
sex chromosomes are the same size) can therefore be ex-
pected in many dioecious angiosperms, because not enough
time has passed for them to differentiate morphologically (see
section on degeneration below). As the sex chromosomes are
often expected to be homomorhpic, genetic markers would
be required for their detection (because cytology can only
identify heteromorphic sex chromosomes) and this could ex-
plain why so few of them have been identified. In angio-
sperms, dioecy evolved independently from
hermaphroditism somewhere between 871 and 5000 times
(
Renner 2014). Therefore, it is likely that many sex chromo-
some systems are yet to be discovered in plants, along with
the mechanism for their origin.
There is evidence that plant sex chromosomes derive from
apairofautosomes(
Nicolas et al. 2005; Filatov 2005; Bergero
and Charlesworth 2009
). Theory predicts that at least two
closely linked sex-determining genes are necessary for the
birth of sex chromosomes; the so-called “two-gene model”
(
Charlesworth and Charlesworth 1978;seefig. 2): a male
sterility mutation (recessive in X/Y systems, dominant in Z/W
systems) and a female sterility mutation (dominant in X/Y sys-
tems, recessive in Z/W systems). In UV systems, the dominance
of mutations does not matter as sex is expressed in the haploid
phase (
fig. 1c).
Some studies have revealed the possibility of the “two-
gene model” occurring in plants. For example, in the subdioe-
cious plant Fragaria virginiana, the male function region and
the female function region have been mapped to the same
linkage group, separated by approximately 6 cM and recom-
bination between the two loci was shown to lead to hermaph-
rodites and neuters (both male and female sterile) in cross
progenies (
Spigler et al. 2008). The name given to sex chro-
mosomes at this first stage of their evolution is “proto-sex
chromosomes” (
fig. 2a). In Fragaria virginiana, because the
mutation causing male sterility is dominant and the one caus-
ing female sterility is recessive, the system consists of proto-
ZW sex chromosomes. Another example is the papaya, where
hermaphrodites are determined by a Y
h
-specific region that
recently evolved (around 4000 years ago) from a much older Y
specific region (that evolved around 9 million years, hereafter
My, ago), possibly after the loss of the dominant female ste-
rility mutation (
VanBuren et al. 2015). However, further ge-
netic analyses will be necessary to confirm the two-gene
model in this species. In Silene latifolia, the X/Y chromosomes
are heteromorphic and mutants with deletions on the Y have
revealed that there are two to three main sex-determining
regions (at least one female-suppressing and at least one
male-promoting), as expected under the (at-least) “two-
gene model” (
Zluvova et al. 2007; Bergero et al. 2008;
Kazama et al. 2016). The genes, however, still remain to be
identified.
So far, only two plant sex-determining genes have been
identified as being located on sex chromosomes. One (called
MID) functions in the green algae Volvox carteri to govern
gametic differentiation and is only present in the minus hap-
lotype (
Ferris and Goodenough 1997). Another sex-determin-
ing gene is OGI, a small RNA-encoded on the Y specific region
of the crop species Diospyros lotus (persimmon). OGI has
male-specific expression and was found to down-regulate
the expression of MeGi; a gene that represses male function
(
Akagi et al. 2014). However, MeGi is autosomal and there-
fore the interplay between MeGi and OGI does not fit well
with the “two-gene model,” unless another yet unknown Y
gene has a female-sterility mutation (
Renner 2016). For other
species, candidate sex-determining genes have been pro-
posed but their location on sex chromosomes has yet to be
assessed. For instance in Asparagus officinalis, pollen develop-
ment aborts late in females at the microspore maturation
stage, and
Harkess et al. (2015) showed that the AMS
(Aborted Microspores) gene has male-biased expression.
This makes this species a good candidate for finding a male
sterility gene, as this same gene is known to be involved in
microspore maturation in another plant (Arabidopsis thaliana),
but further analyses are required to evaluate whether this
gene is indeed located on the Y chromosome for Asparagus
officinalis.
Plant Sex Chromosome Evolution GBE
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FIG.2.—Example progression of XY sex chromosome evolution. Note that this is only one potential evolutionary pathway, not all stages are obligatory
and each stage of the pathway is not necessarily associated with the age of the system. In (a), the YY genotype is viable and only sex-determining genes differ
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There are other known sex-determining genes in plants,
but they all come from monoecious cucurbits (
Boualem
et al. 2008
, 2009, 2015; Martin et al. 2009); monoecious
meaning that male and female flowers are on a single
plant tha t does not have sex chromosomes. In these
plants the WIP1 gene inhibits female function when
active, but WIP1 can be inhibited by another gene
(ACS11). By fixing a recessive loss-of-function mutation in
ACS11, and maintaining WIP1 as polymorphic with a func-
tional and a nonfunctional allele,
Boualem et al. (2015)
created an artificial dioecious population of melons
(Cu cumis melo) and maintained it over time. This experi-
ment demonstrated that dioecy can be determined by a
single gene, because only the WIP1 gene determines the
sex of individuals once a loss-of-function mutation is fixed
in ACS11. It remains unknown however, whether these
mutations have been recruited in closely related dioecious
species with sex chromosomes. If they have been, this
would not fit the “two-gene model.”
The “two-gene model” and the evolutionary pathway
leading to dioecy through gynodioecy (the coexistence of
females and hermaphrodites within a species) could explain
why in angiosperms, XY systems seem to be more frequent
than ZW (
Ming et al. 2011). However, as the above exam-
ples indicate, it is unclear how widespread the “two-gene
model” is in reality for angiosperms and alternative models
could exist in dioecious plants (
Renner 2016). Also, given
that there are few angiosperms with an identified sex chro-
mosome system, the prevalence of XY systems could be due
to a sampling bias.
The Differentiation of Sex Chromosomes
Once proto-sex chromosomes have established, they can con-
tinue to differentiate into sex chromosomes through a
number of different mechanisms. Several species of plants
and algae have sex chromosomes that show varying degrees
of differentiation, each of which could represent different
stages of sex chromosome evolution (
fig. 2). Fragaria virgini-
ana could be seen as representing the first stage of differen-
tiation. Recombination events between the two sex-
determining loci of their proto-Z and proto-W generate neu-
ters and hermaphrodites (
Spigler et al. 2008). In this species,
neuters are selected against as they cannot reproduce, and
hermaphrodites are expected to be selected against if they
have a lower fitness compared with males and females.
Theory predicts that this scenario would select for
recombination suppression between the two sex-determining
loci and the proto-sex chromosomes would be transformed
into actual sex chromosomes. As a consequence, the male-
specific region of the Y chromosome would stop recombining
and become a sex-specific nonrecombining region (hereafter
SNR). Genes located in the SNR and/or its X-homologous
region are called sex-linked genes. The PAR (pseudoautosomal
region) surrounding the SNR would continue to recombine in
both males and females, but the SNR-homologous region on
the X would continue to recombine only in females. This early
stage of sex chromosome evolution after recombination sup-
pression between the two sex-determining genes can be ob-
served in the plant Asparagus officinalis (
fig. 2b; Telgmann-
Rauber et al. 2007
). The process unfolds in the same way for
ZW systems, the only difference being that the female-specific
region on the W does not recombine. In UV systems, both
male-specific and female-specific regions do not recombine as
the sporophyte is always heterogametic.
Unlike Asparagus officinalis, many species with sex chro-
mosomes have much larger SNRs than the expected small
region containing the two closely linked sex-determining
genes, which suggests that sex chromosomes undergo further
recombination suppression events. This has been confirmed at
the molecular level by the study of X-Y, Z-W, or U-V diver-
gence, whenever sequences are available (see
Box 1 for sex
chromosome sequencing methods). Indeed, after recombina-
tion suppression, SNRs accumulate substitutions separately
and, using a molecular clock approach, it is possible to esti-
mate the time when recombination stopped. Because sex-
linked genes with similar X-Y, Z-W, or U-V divergence levels
tend to be located in similar genomic regions (called strata),
unless these regions have later been rearranged, one can infer
that for each strata, recombination was suppressed at rela-
tively different points in time. For example, in Silene latifolia,
there have been at least two recombination suppression
events (
Nicolas et al. 2005) as genes fall into at least two
categories of X-Y divergence. Recombination suppression
also seems to be associated with chromosomal rearrange-
ments, in particular with inversions. For example, in papaya
two large inversion events appear to define the two strata
present in this species (Wang et al. 2012). Several additional
studies have revealed much variation in the characteristics and
abundance of strata in plant and algal species (reviewed in
Table 1).
But what is the evolutionary force driving these additional
events of recombination suppression on sex chromosomes?
FIG.2.—Continued
(as shown on the zoom). Recombination can be suppressed in the immediate area around the sex-determining genes (b) or further suppressed along flanking
regions (c), this can lead to the accumulation of repeated elements and a consequent increase in size of the Y (d). The Y chromosome can also become
smaller than the X chromosome through deletions in the SNR (d1.1)(
Segawa et al. 1971). Neo-sex chromosomes can evolve with reciprocal translocation
(d2)(Howell et al. 2009) or with X autosome fusion (d3), (Smith 1964). Example organisms exhibiting each stage are given in parentheses. Recombining
regions are indicated with crossed double-ended arrows.
Plant Sex Chromosome Evolution GBE
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