Hormonal Regulation of Sex Expression in Plants

Unlike most animal species that can travel in search for food and breeding partners, higher plants cannot move from their rooting position. As a consequence, it is likely that the present lifestyle of higher plants reflects their practical adaptation to the environment. To survive stressful environmental conditions that prevail on uplands, higher plants have evolved various organs such as roots, stems, leaves, and flowers. Flowers are the sexual organs that are used to produce progeny, and they have evolved mechanisms for promoting genetic diversity. For most species of flowering plants, cross-pollination (allogamy) is the best way to avoid inbreeding depression and to promote hybrid vigor. Of the approximately 120,000 known species of flowering plants, 72% produce bisexual flowers while 28% produce unisexual flowers (Yampolsky and Yampolsky, 1922). Approximately one-tenth of flowering plant species are absolutely dioecious or monoecious (4 and 7%, respectively). Seven percent of species show intermediate forms of sexual dimorphism, including gynodioecy and androdioecy, whereas 10% of species contain both unisexual and bisexual flowers. Dioecious species produce male or female flowers on separate individual plants. Monoecious species produce male and female flowers on the same plant. Although the percentage of species producing unisexual flowers is lower than that of the species producing bisexual flowers, some well-known and strategically important plants are either dioecious or monoecious. For example, maize (Zea mays), cucumber (Cucumis sativus), melon (Cucumis melo), and fig (Ficus carica) are monoecious species, while asparagus (Asparagus officinalis), spinach (Spinacia oleracea), hemp (Cannabis sativa), mercury (Mercurialis annua), and hop (Humulus lupulus) are dioecious. For these plants, spatial separation of the sexual organs promotes allogamy. In dioecious plants, there are three different types of sex determination. Firstly, there is the active-Y system. In dioecious melandrium (Silene latifolia = Melandrium album) and cannabis (C. sativa), the Y chromosome is the primary factor that defines sex (Ainsworth et al., 1998; Dellaporta and Calderon-Urrea, 1993); male plants are heterogametic, displaying XY, whereas female plants are homogametic, displaying XX. The Y chromosome contains genes necessary for suppressing female expression, inducing stamen development and maturing anthers. Higher X copy number overcomes the Y chromosome masculinization effect, suggesting that the factors that suppress male expression exist on the X chromosome. Secondly, there is the X-to-autosome (X:A) balance system. The sex expression of approximately 10 dioecious species that belong to Rumex acetosa is classified under this system. In the X:A system, female plants are denoted 2n = 12 + XX (X:A = 1.0), whereas male plants are denoted 2n = 12 + XY₁Y₂ (X:A = 0.5). Polyploid analysis indicates that female flowers are induced when the X-to-autosome ratio is 1.0 or higher, whereas male flowers are induced when the X-to-autosome ratio is 0.5 or lower. Where ratios fall between 0.5 and 1.0, intersex (partial male/female) or hermaphrodite plants occur. The X-to-autosome ratio also applies to the sex expression of dioecious hop (H. lupulus). Thus, sex expression in these dioecious plants has been thoroughly investigated and elucidated with respect to sex chromosomes. Finally, dioecious plants of the third category do not have sex chromosome. For example, sex inheritance in dioecious mercury (M. annua) cannot be explained by heterochromosome and it has been proposed that three genes (A, B₁, and B₂) control sex expression of mercury plants (Louis, 1989). Mercury plants that harbor a dominant A gene and one of the dominant B genes, i.e., A/- B₁/- and A/- B₂/-, exhibit male predominance. In contrast, femaleness in mercury plants is increased by the presence of either a dominant A gene or one of the dominant B genes alone (i.e., A/A b₁/b₁ b₂/b₂, a/a B₁/B₁ b₂/b₂, and a/a b₁/b₁ B₂/B₂). Since there is an excellent previous review of sex determination in mercury plants (Durand and Durand, 1991), it is not discussed further in this review. In higher plants, it is known that plant hormones such as auxin, cytokinin, gibberellins, abscisic acid, and ethylene pleiotropically regulate plant growth and development. These plant hormones also affect sex differentiation in some monoecious and dioecious plants. For example, auxin induces female flower expression in cucumber, melon, and hemp but promotes male flower expression in hop and mercury. Similarly, gibberellins induce female flowers in maize but male flowers in cucumber, melon, asparagus, and hemp. Therefore, as exemplified by these, certain plant hormones can have opposing effects on sex differentiation for different plants. In cucumber, melon, and hemp, ethylene and auxin mediate feminization, whereas gibberellins induce masculinization. In maize, asparagus, and hop, only one plant hormone is effective in inducing sexualization. In conclusion, there is no plant hormone that exhibits a generalized effect in determining the sexuality of monoecious and dioecious plants. The corollary of this observation is that each monoecious and dioecious plant must possess its own mechanism for hormonally regulating sex expression. In particular, monoecious plants that lack sex chromosomes have been the subject of several studies on the evolution and developmental mechanisms of sexual differentiation in higher plants. This review focuses mainly on the hormonal regulation of sex expression in monoecious plants, with particular emphasis on maize (Z. mays) and cucumber (C. sativus). We also discuss the mutual and different aspects of the regulatory systems that control their sex expression and present a genetic model of sex expression in maize and cucumber plants.