Sex-Determining Mechanisms in Land Plants

Abstract

Sex determination is a process that leads to the physical separation of male and female gamete-producing structures to different individuals of a species. Even though sexually reproducing species have only three possible options—to relegate the two sexes to separate individuals, to keep them together on the same individual, or to have a combination of both—plants in particular display a great variety of sexual phenotypes. In angiosperms, a sex-determining process is manifest in species that are monoecious, in which at least some flowers are unisexual but the individual is not, or dioecious, in which unisexual plants produce flowers of one sex type. In plants that produce no flowers and are homosporous, sex determination is manifest in the gametophyte generation with the production of egg- and sperm-forming gametangia on separate individual gametophytes. The determinants of sexual phenotype in plants are diverse, ranging from sex chromosomes in Marchantia polymorpha and Silene latifolia to hormonal regulation in Zea mays and Cucumis sativa to pheromonal cross-talk between individuals in Ceratopteris richardii. Here, we highlight recent efforts aimed at understanding the genetic and molecular mechanisms responsible for sex determination in several plant species that separate their sexes into two individuals or flowers. Representatives of all major land plant lineages are included to give an evolutionary perspective, which is important in understanding how different sex-determining mechanisms evolved and their consequences in plant development and evolution. Although great progress has been made in genetically identifying the genes that regulate sex expression in these species, few of them have been cloned. Because a “one-size-fits-all” mechanism of sex determination will not account for the variety of sexual systems in plants, future efforts at cloning these genes in several well-chosen model systems will be necessary to understand these processes at the molecular level. There are several excellent recent reviews of sex determination that describe species that have not been included to which the reader is directed (Ainsworth, 1999, 2000; Geber et al., 1999; Matsunaga and Kawano, 2001; Negrutiu et al., 2001; Barrett, 2002; Charlesworth, 2002). We begin with the most basal lineage of the land plants. The Life Cycle of the Liverwort Marchantia polymorpha. Haploid gametophytes develop gametangia in antheridiophores and archegoniophores that produce the sperm and egg, respectively. Upon fertilization, which is facilitated by raindrops, the diploid sporophyte remains attached to the archegoniophore and produces yellow sporangia, in which haploid spores are formed after meiosis. The spores are liberated and germinate to form a new gametophyte thallus. The sex of the thallus depends on which sex chromosome it inherits. Photographs courtesy of Katsuyuki Yamato, Kyoto University. In many species of bryophytes, heterothallism (unisexuality) has been correlated with the presence of sex chromosomes (Smith, 1955). Although the extent of heterothallism and sex chromosomes in the bryophytes has not been assessed systematically, this is the only known group of homosporous plants that uses sex chromosomes in sex determination. To date, studies of bryophyte sex determination have focused on the heterothallic liverwort Marchantia polymorpha. In this species, the male and female thalli (vegetative gametophytes) look alike, although males and females can be distinguished easily by differences in the morphology of the sexual structure each produces. A gametophyte bears gametangia on stalked branches called antheridiophores (if male) or archegoniophores (if female) that arise from the upper surface of the thallus (Figure 1). Antheridiophores produce sperm-forming antheridia, and archegoniophores produce egg-forming archegonia. The sex of each haploid gametophyte is determined by cytologically distinct sex chromosomes, with males having one very small Y chromosome and no X chromosome and females having one X chromosome and no Y chromosome (Lorbeer, 1934). In addition to its rapid growth (it is often an invasive weed in greenhouses), its ability to be propagated vegetatively by gemma cups (Figure 1), and its ability to be transformed (Takenaka et al., 2000), Marchantia has a relatively small genome size of 280 Mbp distributed among eight autosomes plus one sex chromosome (Okada et al., 2000), making it a worthy model organism amenable to genomics-style investigations. Working on the assumption that sex-determining factors exist on the Marchantia sex chromosomes, Okama and colleagues (2000) set out to identify these factors by constructing separate male and female P1-derived artificial chromosome (PAC) libraries and identifying clones specific to either the male or the female genome. Their screen resulted in 70 male-specific PAC clones that hybridized only the Y chromosome by fluorescence in situ hybridization. No female-specific clone