Abstract
Monoecious and andromonoecious cultivars of watermelon are characterised by the production of male and female flower or male and hermaphrodite flowers, respectively. The segregation analysis in the offspring of crosses between monoecious and andromonoecious lines has demonstrated that this trait is controlled by a single gene pair, being the monoecious allele M semi-dominant to the andromonoecious allele A. The two studied F1 hybrids (MA) had a predominantly monoecious phenotype since both produced not only female flowers, but also bisexual flowers with incomplete stamens, and hermaphrodite flowers with pollen. Given that in other cucurbit species andromonoecy is conferred by mutations in the ethylene biosynthesis genes CmACS7, CsACS2 and CpACS27A we have cloned and characterised CitACS4, the watermelon gene showing the highest similarity with the formers. CitACS4 encoded for a type ACS type III enzyme that is predominantly expressed in pistillate flowers of watermelon. In the andromonoecious line we have detected a missense mutation in a very conserved residue of CitACS4 (C364W) that cosegregates with the andromonoecious phenotype in two independent F2 populations, concomitantly with a reduction in ethylene production in the floral buds that will develop as hermaphrodite flowers. The gene does not however co-segregates with other sex expression traits regulated by ethylene in this species, including pistillate flowering transition and the number of pistillate flowers per plant. These data indicate that CitAC4 is likely to be involved in the biosynthesis of the ethylene required for stamen arrest during the development of female flowers. The C364W mutation would reduce the production of ethylene in pistillate floral buds, promoting the conversion of female into hermaphrodite flowers, and therefore of monoecy into andromonoecy.
Highlights
The cultivated species of the Cucurbitaceae family, including melon, cucumber, watermelon, squash and gourds, are monoecious, developing unisexual male and female flowers on the same individual plant
The female flowers with no stamen development were scored as AI = 1, while hermaphrodite flowers with complete stamens and pollen were scored as AI = 3
Studies on the inheritance of watermelon sex morphotypes have indicated that monoecy is dominant to andromonoecy and controlled by a single gene with two alleles [6, 8, 37]
Summary
The cultivated species of the Cucurbitaceae family, including melon, cucumber, watermelon, squash and gourds, are monoecious, developing unisexual male and female flowers on the same individual plant. The predominant monoecious cultivars coexist with partially andromonoecious ones [9], and some androecious mutants have been recently described [10, 11], but no gynoecious squash have been identified so far Sex determination in this family is mainly controlled by the gaseous hormone ethylene. The andromonoecious morphotype in cucumber, melon and zucchini squash, result from mutations in the three orthologous ethylene biosynthesis genes CmACS7, CsACS2 and CpACS27A, respectively [9, 18, 19]. These genes are expressed only in pistillate flower primordia and are responsible for the arrest of stamens during the development of unisexual female flowers. They correspond to CmACS11 and CsACS11, both involved in the biosynthesis of ethylene in the phloem of flowers programmed to become females, and in melon this gene functions as a negative regulator of the male-promoting transcription factor gene CmWIP1 [24]
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