Potential Involvement of Cell Cycle-Related Genes in the Arrest of Stamen Development of Female Flowers During Sex Expression in Cucumber (Cucumis sativus L.)

Cucumber (Cucumis sativus L.) has been used as a model higher plant for the study of sex expression (Galun, 1961; Shifriss, 1961; Kubicki, 1969a; 1969b; Malepszy and Niemirowicz-Szczytt, 1991). Sex expression in cucumber plants is genetically controlled by the F and M genes. These genes interact to produce four different sex phenotypes: gynoecious (M-F-), monoecious (M-ff), hermaphroditic (mmF-), and andromonoecious (mmff). Gynoecious cucumber plants produce only female flowers; monoecious plants produce both male and female flowers; hermaphroditic plants produce bisexual flowers with both staminate and pistillate organs; and andromonoecious plants produce bisexual and male flowers. Of these various sex phenotypes, monoecious is the most common type of sex expression in cucumber plants. Morphologically, all flower buds in monoecious cucumber plants contain both stamen and pistil primordia at the early stage of their differentiation, and later develop into male or female flowers. Pistil development is arrested in flower buds destined to become male flowers, whereas stamen development is arrested in flower buds that become female flowers (Kubicki, 1969c; Yamasaki et al., 2005). Sex differences are thus established by the selective arrest of sexual organ primordia in monoecious cucumber plants. In cucumber, sex expression can be regulated not only by the genetic loci described above, but also by plant hormones and environmental conditions (Atsmon and Galun, 1960; Shifriss and George, 1964; Frankel and Galun, 1977; Takahashi et al., 1983; Durand and Durand, 1984). In particular, production of the plant hormone ethylene is highly correlated with femaleness in cucumber plants, for example, gynoecious cucumber plants produce more ethylene than monoecious plants (George, 1971; Rudich et al., 1972; Trebitsh et al., 1987). In addition, inhibitors of ethylene biosynthesis or ethylene action suppress the development of female flowers and induce male flowers (Beyer, 1976; Atsmon and Tabbak, 1979; Takahashi and Suge, 1980; Takahashi and Jaffe, 1984; Yamasaki et al., 2000; Yamasaki and Manabe, 2011). Furthermore, application of ethylene to monoecious cucumber plants promotes the formation of female flowers (MacMurray and Miller, 1968; Iwahori et al., 1970; Takahashi and Suge, 1980; 1982; Yamasaki et al., 2000). These physiological phenomena were confirmed at the molecular level. Two genes (CSACS1G and CS-ACS2) which encode a key enzyme in the ethylene biosynthesis pathway, 1-aminocyclopropane-1carboxylic acid (ACC) synthase, were identified as being related to sex expression in cucumber plants. The CSACS1G gene, which exists in gynoecious cucumber plants but not in monoecious cucumber plants, was closely linked to the F gene (Trebitsh et al., 1997). The CS-ACS2 gene