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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
In situ hybridization using RhAG antisense probe on early stage flowers of cultivated roses and their likely wild ancestor.(A–C) Pattern of RgAG expression in flowers of R. gallica (a simple flower rose) at development stage 4 (A) and in flowers of R. gallica “Cardinal de Richelieu” (double flower) (B, C), at development stage 5. Note that RgAG expression pattern is weaker and is restricted to the central whorl (carpel domain) in “Cardinal de Richelieu”, thus in accordance to the pattern observed in “Malmaison”. (D–F) Pattern of RcAG expression in R. chinensis “mutabilis” (D) a cultivated simple flower variety that was used as a model for wild-type R. chinensis, and its genetically related semi-double flower rose R. chinensis “Old Blush” (E,F) In “Mutabilis” at stage 5 of development, RcAG mRNA accumulates in a wide area corresponding to whorls 3 and 4. In “Old Blush” at stage 3 of development (E) RhAG expression is detected in the center of the flower, whereas at stage 5 (F), RcAG pattern of expression is partially restricted towards the center of the flower, giving rise to semi-double corolla. (G,H) Pattern of RrAG expression in R. rugosa around stage 4 of development (G), a simple flower rose (5 petals) and (H) its genetically related hybrid descendant R. rugosa “Roseraie de l'Haÿ” (semi-double corolla). Scale bar (A–H)  = 200 micrometers
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pone-0009288-g006: In situ hybridization using RhAG antisense probe on early stage flowers of cultivated roses and their likely wild ancestor.(A–C) Pattern of RgAG expression in flowers of R. gallica (a simple flower rose) at development stage 4 (A) and in flowers of R. gallica “Cardinal de Richelieu” (double flower) (B, C), at development stage 5. Note that RgAG expression pattern is weaker and is restricted to the central whorl (carpel domain) in “Cardinal de Richelieu”, thus in accordance to the pattern observed in “Malmaison”. (D–F) Pattern of RcAG expression in R. chinensis “mutabilis” (D) a cultivated simple flower variety that was used as a model for wild-type R. chinensis, and its genetically related semi-double flower rose R. chinensis “Old Blush” (E,F) In “Mutabilis” at stage 5 of development, RcAG mRNA accumulates in a wide area corresponding to whorls 3 and 4. In “Old Blush” at stage 3 of development (E) RhAG expression is detected in the center of the flower, whereas at stage 5 (F), RcAG pattern of expression is partially restricted towards the center of the flower, giving rise to semi-double corolla. (G,H) Pattern of RrAG expression in R. rugosa around stage 4 of development (G), a simple flower rose (5 petals) and (H) its genetically related hybrid descendant R. rugosa “Roseraie de l'Haÿ” (semi-double corolla). Scale bar (A–H)  = 200 micrometers

Mentions: We analyzed the pattern of expression of the rose AGAMOUS orthologs by in situ hybridization on longitudinal sections of early developing flowers (Figure 6). In R. gallica ‘Cardinal de Richelieu’, RgAG (Rg for Rosa gallica) expression pattern was restricted to whorl 4, whereas it was present in both whorls 3 and 4 in its wild-type ancestor R. gallica (Figure 6A, C). These data suggest that during domestication of R. gallica the selection of double flower phenotype could have occurred through the restriction of RgAG expression.


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)

In situ hybridization using RhAG antisense probe on early stage flowers of cultivated roses and their likely wild ancestor.(A–C) Pattern of RgAG expression in flowers of R. gallica (a simple flower rose) at development stage 4 (A) and in flowers of R. gallica “Cardinal de Richelieu” (double flower) (B, C), at development stage 5. Note that RgAG expression pattern is weaker and is restricted to the central whorl (carpel domain) in “Cardinal de Richelieu”, thus in accordance to the pattern observed in “Malmaison”. (D–F) Pattern of RcAG expression in R. chinensis “mutabilis” (D) a cultivated simple flower variety that was used as a model for wild-type R. chinensis, and its genetically related semi-double flower rose R. chinensis “Old Blush” (E,F) In “Mutabilis” at stage 5 of development, RcAG mRNA accumulates in a wide area corresponding to whorls 3 and 4. In “Old Blush” at stage 3 of development (E) RhAG expression is detected in the center of the flower, whereas at stage 5 (F), RcAG pattern of expression is partially restricted towards the center of the flower, giving rise to semi-double corolla. (G,H) Pattern of RrAG expression in R. rugosa around stage 4 of development (G), a simple flower rose (5 petals) and (H) its genetically related hybrid descendant R. rugosa “Roseraie de l'Haÿ” (semi-double corolla). Scale bar (A–H)  = 200 micrometers
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2823793&req=5

pone-0009288-g006: In situ hybridization using RhAG antisense probe on early stage flowers of cultivated roses and their likely wild ancestor.(A–C) Pattern of RgAG expression in flowers of R. gallica (a simple flower rose) at development stage 4 (A) and in flowers of R. gallica “Cardinal de Richelieu” (double flower) (B, C), at development stage 5. Note that RgAG expression pattern is weaker and is restricted to the central whorl (carpel domain) in “Cardinal de Richelieu”, thus in accordance to the pattern observed in “Malmaison”. (D–F) Pattern of RcAG expression in R. chinensis “mutabilis” (D) a cultivated simple flower variety that was used as a model for wild-type R. chinensis, and its genetically related semi-double flower rose R. chinensis “Old Blush” (E,F) In “Mutabilis” at stage 5 of development, RcAG mRNA accumulates in a wide area corresponding to whorls 3 and 4. In “Old Blush” at stage 3 of development (E) RhAG expression is detected in the center of the flower, whereas at stage 5 (F), RcAG pattern of expression is partially restricted towards the center of the flower, giving rise to semi-double corolla. (G,H) Pattern of RrAG expression in R. rugosa around stage 4 of development (G), a simple flower rose (5 petals) and (H) its genetically related hybrid descendant R. rugosa “Roseraie de l'Haÿ” (semi-double corolla). Scale bar (A–H)  = 200 micrometers
Mentions: We analyzed the pattern of expression of the rose AGAMOUS orthologs by in situ hybridization on longitudinal sections of early developing flowers (Figure 6). In R. gallica ‘Cardinal de Richelieu’, RgAG (Rg for Rosa gallica) expression pattern was restricted to whorl 4, whereas it was present in both whorls 3 and 4 in its wild-type ancestor R. gallica (Figure 6A, C). These data suggest that during domestication of R. gallica the selection of double flower phenotype could have occurred through the restriction of RgAG expression.

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