Academic journal article Genetics

Early Sex-Chromosome Evolution in the Diploid Dioecious Plant Mercurialis Annua

Academic journal article Genetics

Early Sex-Chromosome Evolution in the Diploid Dioecious Plant Mercurialis Annua

Article excerpt

THE evolution of dioecy (separate sexes) from hermaphroditism, which has occurred repeatedly in independent lineages of flowering plants (Renner 2014), is a prelude to the possible evolution of sex chromosomes. Early sex-chromosome evolution typically involves the accumulation of repetitive sequences in a nonrecombining region (J. Wang et al 2012; Hobza et al. 2017), differences in codon use between homologs (Ono 1939; Qiu et al. 2010), different patterns of gene expression at sex-linked loci (Zemp et al. 2016), pseudogenization and gene loss (Papadopulos et al. 2015; Wu and Moore 2015), and, ultimately, divergence in chromosome length between homologs (Puterova et al. 2018). Extreme divergence is common in many animals, but it is also known in some plants in which the homologous chromosomes are heteromorphic and distinguishable by karyotype, e.g., in the plant species Silene latifolia (Ono 1939; Krasovec et al. 2018) and Rumex hastatulus (Smith 1955; Hough et al. 2014). In other plants, the sex chromosomes remain indistinguishable by karyotype, and gene function is only mildly compromised, e.g., Asparagus officinalis (Loeptien 1979; Telgmann-Rauber et al. 2007), Spinacia oleracea (Yamamoto et al. 2014), Diospyros lotus (Akagi et al. 2014), Fragaria chiloensis (Tennessen et al. 2016), Populus (Geraldes et al. 2015), Carica papaya (Horovitz and Jiménez 1967; Liu et al. 2004), and Salix (Pucholt et al. 2015). Because of this variation, and because dioecy in plants has often evolved recently, plants with young homomorphic sex chromosomes provide particularly good models for studying the very earliest stages in sexchromosome divergence (Charlesworth 2016).

Two hypotheses have been proposed to explain the suppression of recombination in plants. First, if dioecy evolves through the spread of male- and female-sterility mutations, these mutations must become linked on opposite chromosomes to avoid the expression of either hermaphroditism, or both male and female sterility simultaneously (Charlesworth and Charlesworth 1978). The main experimental support for this two-locus model comes from classic genetic studies in S. latifolia (Westergaard 1958) that demonstrated the presence of two sex-determining factors on the Y-chromosome: the stamen-promoting factor (SPF) and gynoecium suppression factor (GSF). More recent work mapped the location of these genes on the S. latifolia Y-chromosome (Kazama et al. 2016), although the actual GSF and SPF genes have yet to be identified. Nevertheless, although there is some support for it, the two-locus model does not explain why nonrecombining regions on sex chromosomes often expand greatly (Bergero and Charlesworth 2009), well beyond the region harboring the original sex-determining genes.

A second hypothesis invokes selection favoring suppressed recombination between a sex-determining locus and loci elsewhere on the sex chromosome that have different allelic effects on the fitness of males and females, i.e., alleles with sexually antagonistic effects (Rice 1987; Charlesworth 1991; Gibson et al. 2002; Charlesworth et al. 2005; Bergero and Charlesworth 2009). The suppression of recombination is expected to extend consecutively to generate linkage between the sexdetermining locus and more sexually antagonistic loci (Charlesworth 2015), and these extensions can be identified as discrete "strata," with greater X/Y divergence in strata that ceased recombining earliest. Evidence for strata has been found both in animals (Lahn and Page 1999; Nam and Ellegren 2008) and plants (Bergero et al. 2007; K. Wang et al. 2012), but there is still little direct evidence for the role played by sexually antagonistic selection in bringing them about (Bergero et al. 2019). A recent study of guppy sex chromosomes claimed evidence for the evolution of strata consistent with the sexual-antagonism hypothesis (Wright et al. 2017), but subsequent work has shown that strata could actually not have been involved in the evolution of suppressed recombination (Bergero et al. …

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