Tinkering with the C-Function: A Molecular Frame for the Selection of Double Flowers in Cultivated Roses

Abstract

BackgroundRoses have been cultivated for centuries and a number of varieties have been selected based on flower traits such as petal form, color, and number. Wild-type roses have five petals (simple flowers), whereas high numbers of petals (double flowers) are typical attributes of most of the cultivated roses. Here, we investigated the molecular mechanisms that could have been selected to control petal number in roses.Methodology/Principal FindingsWe have analyzed the expression of several candidate genes known to be involved in floral organ identity determination in roses from similar genetic backgrounds but exhibiting contrasting petal numbers per flower. We show that the rose ortholog of AGAMOUS (RhAG) is differentially expressed in double flowers as compared to simple flowers. In situ hybridization experiments confirm the differential expression of RhAG and demonstrate that in the double-flower roses, the expression domain of RhAG is restricted toward the center of the flower. Conversely, in simple-flower roses, RhAG expression domain is wider. We further show that the border of RhAG expression domain is labile, which allows the selection of rose flowers with increased petal number. Double-flower roses were selected independently in the two major regions for domestication, China and the peri-Mediterranean areas. Comparison of RhAG expression in the wild-type ancestors of cultivated roses and their descendants both in the European and Chinese lineages corroborates the correlation between the degree of restriction of RhAG expression domain and the number of petals. Our data suggests that a restriction of RhAG expression domain is the basis for selection of double flowers in both the Chinese and peri-Mediterranean centers of domestication.Conclusions/SignificanceWe demonstrate that a shift in RhAG expression domain boundary occurred in rose hybrids, causing double-flower phenotype. This molecular event was selected independently during rose domestication in Europe/Middle East and in China.

Flower and early fruit development in a diploid strawberry, Fragaria vesca

“…Both wild rose and Fragaria Xowers develop Wve petals, a large number of stamens and apocarpous gynoecium. However, rose Xowers are perigynous meaning that the multiple apocarpous pistils are initiated from a Xat receptacle base buried within a cuplike hypanthium (Dubois et al 2010). The multiple free fruits (seeds) of rose are buried within the enclosed Xeshy hip.…”

“…The early stages of rose Xower development are divided into Wve stages (Dubois et al 2010), which mirror stages 3-7 of F. vesca Xower development. (Fig.…”

Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant

“…Moreover, scientists have put similar natural deviations from normal development to good use to help elucidate the genetic basis of normal flower development (32,33). Although morphological, developmental, and/or genetic aspects of double-flower cultivars have been investigated (22,(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44), no functional evidence for the underlying molecular mechanism of this familiar phenotype is available to date in a noncore eudicot.…”

Thermal Control Suitable for Increasing Petals in <i>Eustoma grandiflorum</i> (Raf.) Shinn.

“…The fluctuation in the petal number due to temperature has been observed in other species, such as roses, carnations, and cyclamen (Garrod and Harris, 1974;Ma et al, 2015;. Double-flower roses and cyclamen mainly result of homeotic conversion from the stamen to petals affected by temperature (Dubois et al, 2010;Ma et al, 2015;. In carnations, high-temperature treatment elevates the number of petals (Garrod and Harris, 1974).…”

“…Double-flower roses mainly result from homeotic conversion from the stamen to petals affected by temperature governing this degree (Dubois et al, 2010;Ma et al, 2015). The fluctuation in petal number coincides with that of the stamen number in cyclamen .…”