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.
Highlights
Artificial selection for certain animal and plant physical traits by breeders was first used by Charles Darwin as a surrogate to describe the natural selection process underlying evolution [1]
Conclusions/Significance: We demonstrate that a shift in rose ortholog of AGAMOUS (RhAG) expression domain boundary occurred in rose hybrids, causing double-flower phenotype
We demonstrate that the increase of petal number in roses is a consequence of a deregulation of expression of the rose ortholog of AGAMOUS
Summary
Artificial selection for certain animal and plant physical traits by breeders was first used by Charles Darwin as a surrogate to describe the natural selection process underlying evolution [1]. Flower traits such as the floral architecture, petal color and recurrent flowering are key characters that have been subjected to artificial selection pressure during the early domestication and the subsequent breeding process. There was no significant gene flow between the diploid Chinese and tetraploid European rose genotypes until the early 19th century when the first triploid hybrids with reduced fertility were produced, from which our modern tetraploid hybrids arose after recurrent backcrosses (Figure 1; [7,8]) Other species, such as R. rugosa Thunb., were not domesticated until the late 19th or early 20th centuries, and contributed to the modern breeding programs for their hardiness and disease resistance properties [7]. We investigated the molecular mechanisms that could have been selected to control petal number in roses
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