Plant sex determination and sex chromosomes

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Heredity (2002) 88, 94–101  2002 Nature Publishing Group All rights reserved 0018-067X/02 $25.00 www.nature.com/hdy

Plant sex determination and sex chromosomes
D Charlesworth
Institute of Cell, Animal and Population Biology, University of Edinburgh, Scotland, UK

Sex determination systems in plants have evolved many times from hermaphroditic ancestors (including monoecious plants withseparate male and female flowers on the same individual), and sex chromosome systems have arisen several times in flowering plant evolution. Consistent with theoretical models for the evolutionary transition from hermaphroditism to monoecy, multiple sex determining genes are

involved, including male-sterility and female-sterility factors. The requirement that recombination should be rare betweenthese different loci is probably the chief reason for the genetic degeneration of Y chromosomes. Theories for Y chromosome degeneration are reviewed in the light of recent results from genes on plant sex chromosomes. Heredity (2002) 88, 94–101. DOI: 10.1038/sj/hdy/6800016

Keywords: dioecy; sex linkage; Y chromosomes; Silene latifolia

Introduction: why are plant sex chromosomes of particularinterest?
The genetic control of sex determination is becoming well understood in several animal systems, particularly Drosophila melanogaster, Caenorhabditis elegans and mammals. In plants, understanding the sex determination system is closely connected with understanding how separate sexes evolved, and current theoretical ideas about this also illuminate the evolution of sex chromosomes.Angiosperms are also of particular interest for empirical studies of sex chromosome evolution, because they probably evolved separate sexes repeatedly and relatively recently. Other plants, particularly Bryophytes (see Okada et al, 2001), also have interesting independently evolved sex chromosomes. In many sexually reproducing plant species (and some animals) all individuals are essentially alike in theirgender condition. Many such ‘sexually monomorphic’ species are hermaphroditic. The term ‘cosexual’ (Lloyd, 1984) is used when individual plants have both sex functions, whether present within each flower (hermaphrodite), or in separate male and female flowers (monoecious). A minority of plant species are ‘sexually polymorphic’, including dioecious species, with separate males and females (Table 1).Many dioecious species with hermaphrodite relatives have evident rudiments of opposite sex structures in flowers of plants of each sex, suggesting recent evolution of unisexual flowers (Darwin, 1877). The low frequency and scattered taxonomic distribution of dioecy and sex chromosomes suggest that cosexuality is the ancestral angiosperm state (Figure 1) (Charlesworth, 1985; Renner and Ricklefs,1995. Sex chromosomes therefore probably evolved repeatedly and quite recently.

In some plant taxa, it is possible to estimate how many times dioecy has evolved, and how long ago. Dioecy probably evolved twice in the Hawaiian genus Schiedia (Weller et al, 1995). The best studied case at present is the large genus Silene, in the same family (Caryophyllaceae). Many Silene species are gynodioeciousand others are hermaphroditic. A phylogeny constructed from internal transcribed spacer (ITS) sequences of nuclear ribosomal RNA genes of Silene species suggests two origins of dioecy in this genus also (Desfeux et al, 1996). Using a molecular clock, these data suggest an age of probably less than 20 million years for the heteromorphic sex chromosomes of the close relatives Silene latifolia and S.dioica. Comparative analysis suggests that dioecious lineages often have short evolutionary lives (Heilbuth, 2000). Thus separate sexes may have evolved more than 100 times in the flowering plants, given that 160 families have dioecious members.

The genetics of sex determination in plants, and plant sex chromosomes
Sex inheritance and sex chromosomes in plants are strikingly similar to those...
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