The Evolution of Sex Chromosomes and Dosage Compensation in Plants

Abstract

Plant sex chromosomes can be vastly different from those of the few historical animal model organisms from which most of our understanding 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 understanding 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 have been found in plants, and these are hypothesized to be representing different stages of sex chromosome evolution. 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 to 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 that 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.

Keywords: Y degeneration; dioecy; sex chromosome sequencing; sex chromosome turnover; sex-biased expression.

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.

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 (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.

Fig. 4.—

Mechanisms of sex chromosome turnover and absence/presence of recombination suppression: sex-antagonistic genes can induce recombination suppression if located on the PAR (a), resulting in larger SNRs and heteromorphic sex chromosomes (${\text{SA}}_{\mathrm{M}}^2$ here is a male beneficial sex-antagonistic gene that induces further recombination suppression (b) of the Y SNR). The accumulation of deleterious mutations on SNRs following recombination suppression can induce a sex chromosome turnover (c), possibly with endless cycles (but neither from an XY pair to a ZW pair nor from ZW to XY). Sex chromosomes can also be replaced by a new pair (d) if sex-antagonistic genes are located on autosomes (with this mechanism a change of system is possible, from ZW to XY and conversely, but the new pair can only replace a very young sex chromosome pair). The fountain of youth (e) could maintain sex chromosomes at a homomorphic state through X-Y (or Z-W) recombination in sex-reverted individuals.

Fig. 3.—

Available methods for sequencing sex chromosomes, see Box 1 for more details. (a) Vicoso and Bachtrog (2011); Vicoso, Kaiser, et al. (2013); Vicoso, Emerson, et al. (2013), (b) Carvalho and Clark (2013), (c) Gautier (2014), (d) Cortez et al. (2014), (e) Muyle et al. (2016), (f) Hou et al. (2015). Sex chromosome system and required data are indicated with black filled circles when applicable and necessary, respectively, empty circles when not applicable/not necessary, or grey filled circles where only one of two options is required. Chr = Chromosome, RG = Reference Genome, >80 = more than 80 individuals, and “cross” refers to the requirement of parental and offspring data.

Fig. 5.—

Sex antagonism and evolution of gene expression level (made after Barrett and Hough 2013): A hypothetical scenario in which females (red) and males (blue) have different optima for the same trait, causing sex-biased selection (blue and red arrows). A shared genetic architecture can constrain the sexes from evolving toward their respective trait optima (grey arrows). However, sexual dimorphism can still evolve when such trade-offs exist, and this can involve sex-limited gene expression and the breakdown of strong intersexual genetic correlations, possibly facilitated by the evolution of SNRs.