Evolution of Sex Chromosomes in Plants

Abstract

Sex chromosomes are known from a minority of flowering plants (angiosperms), and from some haploid plants, but the sex‐determining chromosomes of many dioecious plants (i.e. species with the sexual stage individuals being either purely male or female) are either unstudied, or are not morphologically different between the two sexes. Both these observations and the taxonomically scattered distribution of species with sex chromosomes suggest that many plant sex chromosome systems evolved recently and independently in different taxa. A fundamental characteristic of sex chromosome pairs is possession of a nonrecombining region. Some plants may be in an early stage of evolving separate sexes, so that this has not yet evolved. Other plants appear to have small nonrecombining regions, or ‘proto‐sex chromosomes’, whereas a few species have cytologically detectable sex chromosome heteromorphism, and probably have large nonrecombining regions. With modern molecular approaches, these different states can now be identified and studied.

Key Concepts:

  • The evolution of separate sexes (males and females) from an initial state in which individuals have both sex functions requires mutations of at least two genes.

  • Sex chromosome pairs are defined as homologous chromosomes (that pair in meiosis, and part of the pair recombines) but which also include a nonrecombining region involved in sex determination.

  • During the evolution of separate sexes, after male‐ and female‐sterility mutations arise, selection will promote reduced recombination between the different genes, in order to avoid producing sterile individuals (with both male‐ and female‐sterility mutations) that will arise through recombination between the genes.

  • The existence of evolutionary strata (see Glossary) shows that recombination suppression between sex chromosomes has occurred in several distinct events, at different times, and the main hypothesis to explain this is that sexually antagonistic polymorphisms may arise in the recombining regions of sex chromosome pairs, and that this situation again generates selection for reduced recombination.

Keywords: chromosome heteromorphism; genetic sex determination; haploid plants; nonrecombining region; transposable element

Figure 1.

Possibilities for the evolutionary origins of dioecy in a set of species (dioecious lineages indicated by black lines) and reversion to nondioecious ‘cosexual’ states (grey lineages). The sex systems in the extant species are the same in both (a) and (b), but the histories are different. Changes are indicated by ‘lightning bolt’ symbols, with pink indicating evolution of dioecy, and green indicating its loss. (a) Single evolutionary origin and two reversions to nondioecious ‘cosexual’ states, and also an event in which a different gene takes over control of sex determination (blue symbol). In both dioecious species with XY systems, sex‐linked genes will be on homologous linkage groups, reflecting the XY pair of their common ancestor, and divergence between sequences of Y‐ and X‐linked alleles can be high if the ancestor had a nonrecombining region. The ZW species may have a homologous or a nonhomologous sex chromosome, which may or may not involve a nonrecombining region. (b) Two independent origins of dioecy and two reversions, one followed by dioecy reevolving. The two dioecious species with XY systems evolved independently, so that their sex chromosomes may be nonhomologous, and divergence between sequences of Y‐ and X‐linked alleles should be lower than that between X‐ or Y‐linked alleles of the two species (reflecting the fact that Y‐linked sequences stopped recombining after the two species split). The possibilities for the ZW species are the same as in part (a).

Figure 2.

Genetic markers in families and populations, showing how genotyping for dense markers can determine which sex is heterogametic. Markers are indicated by thin vertical lines. Most sex‐linked genes in plants have been discovered by finding loci with Y‐linked markers (shown in blue if they are found only in males, which indicates Y‐linkage). Markers indicated in pink are variants seen in all X chromosomes, whereas markers in black indicate variants that are polymorphic among X chromosomes, but not present in 100% of them. Note that, if a region exists in which the Y has degenerated and lost genes, one could fail to be aware of its existence using this approach, potentially underestimating the ages of old systems. For the human XY pair, for instance, absence of knowledge that an ancient Y‐linked region exists that has lost most genes present on the X means that this approach would produce a sparse region in the X map, due to the fact that variants may not be found in the few remaining corresponding Y‐linked genes.

Figure 3.

Diagram to show various ways in which sex chromosome heteromorphism may arise. (a) A young sex chromosome pair with a pericentric inversion. (b) Expansion of Y chromosome due to repetitive sequence accumulation. (c) Y‐autosome translocation. The top arrangement in part C shows the original X and Y, before the rearrangement, and pairing regions are shown with fine lines between the two chromosomes that pair in meiosis; in male meiosis, only the pseudoautosomal region (PAR) of the sex chromosomes pairs (female meiosis is not affected by the rearrangement). If the ancestral Y chromosome has two PARs, the chromosomes would form a ring in male meiosis, as seen in one subspecies of Humulus lupulus (Ainsworth et al., ), and in a Baccharis species (Asteraceae, Hunziker et al., ).

Figure 4.

DNA sequence divergence between Y‐linked alleles and their X‐linked counterparts in humans ((a), from Skaletsky et al., ) and two plants, Silene latifolia ((b), from Bergero et al., ) and C. papaya ((c), from Wang et al., ). The very different divergence values for genes distant from the boundary of the recombining, or PAR define the ‘evolutionary strata’ in the sex chromosomes of these species.

Figure 5.

Steps in the evolution of separate sexes and sex chromosomes. The diagram shows that, to produce the two sexes, at least two mutations are needed (indicated by ‘lightning’ symbols). The first change is probably a recessive mutation (m) in a stamen‐promoting factor; this ‘femaleness factor’ is indicated in pink, and accounts for the fact that females are the homozygous sex. Once sex chromosomes have evolved, this mutation is restricted to the X chromosome, whereas the Y retains the original M allele. The change from cosexual to male probably involves several mutations with dominant or semidominant effects such that heterozygotes with either the original chromosome, or the X, have increased male function. The diagram shows the simplest possible case, with a single mutation on the homologue of the female‐determining chromosome. It is assumed that the ‘maleness factor’ (indicated in blue) or factors decrease female function; they are thus, in effect, gynoecium suppression factors (often denoted by GSF or SuF). Because recombination creates genotypes with both sterility factors (plants with no fully functional sex parts in their flowers), suppressed recombination between these genes is selectively favoured. When sex chromosomes with suppressed recombination have evolved, the maleness factors will be Y linked. Subsequent male‐benefit mutations (or a succession of partial maleness factors) may accumulate on this chromosome, in regions closely linked to the initial male‐determining region. If they also reduce female function, this will select for suppressed recombination in further Y regions, eventually covering most of the Y chromosome.

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Charlesworth, Deborah(Sep 2013) Evolution of Sex Chromosomes in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0025144]