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Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses.

Dubois A, Raymond O, Maene M, Baudino S, Langlade NB, Boltz V, Vergne P, Bendahmane M - PLoS ONE (2010)

Bottom Line: We show that the rose ortholog of AGAMOUS (RhAG) is differentially expressed in double flowers as compared to simple flowers.We 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.

View Article: PubMed Central - PubMed

Affiliation: Reproduction et Développement des Plantes, Université Lyon, Lyon, France.

ABSTRACT

Background: Roses 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 findings: We 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/significance: We 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.

Show MeSH
Simplified genealogy of roses.Cultivated roses originate from two main regions of domestication, i.e. the peri-mediterranean areas (Europe/Middle-East) and China. Double flowers were selected independently in the European and Chinese lineages. ‘Cardinal de Richelieu’ and ‘Old Blush’ represent examples of double and semi-double flower varieties in the R. gallica and R. chinensis lineages. These two gene pools were kept separated until the early nineteenth century, when they were crossed to obtain triploid hybrids and tetraploid modern varieties.
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pone-0009288-g001: Simplified genealogy of roses.Cultivated roses originate from two main regions of domestication, i.e. the peri-mediterranean areas (Europe/Middle-East) and China. Double flowers were selected independently in the European and Chinese lineages. ‘Cardinal de Richelieu’ and ‘Old Blush’ represent examples of double and semi-double flower varieties in the R. gallica and R. chinensis lineages. These two gene pools were kept separated until the early nineteenth century, when they were crossed to obtain triploid hybrids and tetraploid modern varieties.

Mentions: 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]. In recent times, the study of artificial selection processes continues to help shaping the general concepts and models for evolution [2]. In particular, the study of the genetics of crop domestication has recently made enormous progress [3]. Several essential crop characters (such as yield, plant architecture and shedding) were selected during the early phase of domestication. The current improvement phase focuses on augmented nutritional value and resistance to various abiotic and biotic stresses [3]. The molecular mechanisms controlling these processes are becoming increasingly well understood. Many of the ‘favorable’ mutations selected during domestication affect the activity or the expression patterns of master regulatory genes. Some of the best documented examples are found in grasses, where developmental genes encoding mainly transcription factors such as TB1 and TGA1 [4], [5], were found to be associated with domestication (see [6] for exhaustive review). In ornamental plants, 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. Flower forms with increased number of petals (termed double flowers) were retained for their showy aspect in many domesticated plant families. In Rosaceae, for instance, spontaneous double flower forms were kept and propagated for garden ornament (Prunus, Rosa, Potentilla…). Rose species were domesticated several times independently. The two major areas of rose domestication in the Antiquity were China and the peri-mediterranean area (encompassing part of Europe and Middle East), where R. chinensis Jacq. and R. gallica L. were bred and contributed predominantly to the subsequent selection process (Figure 1). In both cases semi-double (8 to 40 petals) and double flower (over 40 petals) forms were selected. 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]. The 200 years of documented rose breeding history is thus a unique resource to study rose hybrids and their wild ancestors and to pinpoint molecular mechanisms that could have been selected to generate double flowers.


Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses.

Dubois A, Raymond O, Maene M, Baudino S, Langlade NB, Boltz V, Vergne P, Bendahmane M - PLoS ONE (2010)

Simplified genealogy of roses.Cultivated roses originate from two main regions of domestication, i.e. the peri-mediterranean areas (Europe/Middle-East) and China. Double flowers were selected independently in the European and Chinese lineages. ‘Cardinal de Richelieu’ and ‘Old Blush’ represent examples of double and semi-double flower varieties in the R. gallica and R. chinensis lineages. These two gene pools were kept separated until the early nineteenth century, when they were crossed to obtain triploid hybrids and tetraploid modern varieties.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2823793&req=5

pone-0009288-g001: Simplified genealogy of roses.Cultivated roses originate from two main regions of domestication, i.e. the peri-mediterranean areas (Europe/Middle-East) and China. Double flowers were selected independently in the European and Chinese lineages. ‘Cardinal de Richelieu’ and ‘Old Blush’ represent examples of double and semi-double flower varieties in the R. gallica and R. chinensis lineages. These two gene pools were kept separated until the early nineteenth century, when they were crossed to obtain triploid hybrids and tetraploid modern varieties.
Mentions: 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]. In recent times, the study of artificial selection processes continues to help shaping the general concepts and models for evolution [2]. In particular, the study of the genetics of crop domestication has recently made enormous progress [3]. Several essential crop characters (such as yield, plant architecture and shedding) were selected during the early phase of domestication. The current improvement phase focuses on augmented nutritional value and resistance to various abiotic and biotic stresses [3]. The molecular mechanisms controlling these processes are becoming increasingly well understood. Many of the ‘favorable’ mutations selected during domestication affect the activity or the expression patterns of master regulatory genes. Some of the best documented examples are found in grasses, where developmental genes encoding mainly transcription factors such as TB1 and TGA1 [4], [5], were found to be associated with domestication (see [6] for exhaustive review). In ornamental plants, 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. Flower forms with increased number of petals (termed double flowers) were retained for their showy aspect in many domesticated plant families. In Rosaceae, for instance, spontaneous double flower forms were kept and propagated for garden ornament (Prunus, Rosa, Potentilla…). Rose species were domesticated several times independently. The two major areas of rose domestication in the Antiquity were China and the peri-mediterranean area (encompassing part of Europe and Middle East), where R. chinensis Jacq. and R. gallica L. were bred and contributed predominantly to the subsequent selection process (Figure 1). In both cases semi-double (8 to 40 petals) and double flower (over 40 petals) forms were selected. 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]. The 200 years of documented rose breeding history is thus a unique resource to study rose hybrids and their wild ancestors and to pinpoint molecular mechanisms that could have been selected to generate double flowers.

Bottom Line: We show that the rose ortholog of AGAMOUS (RhAG) is differentially expressed in double flowers as compared to simple flowers.We 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.

View Article: PubMed Central - PubMed

Affiliation: Reproduction et Développement des Plantes, Université Lyon, Lyon, France.

ABSTRACT

Background: Roses 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 findings: We 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/significance: We 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.

Show MeSH