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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
Longitudinal sections of floral meristems and flowers during floral organogenesis.(A–J) Sections (stained with toluidine blue) of “Malmaison” (A–D,I) and “St Anne's” (E–H, J) were observed, from the floral meristem stage (stage 1; A, E) until carpel formation (stage 4, I, J). Scale bar equals 150 µm for A to H and 1 mm for I and J. (K) Analysis of floral organogenesis in “Malmaison” (top) and “St Anne's” (bottom). Sepals, petals, stamens and carpels are labeled in yellow, green, blue and red colors, respectively. The different whorls composition is displayed as follows: whorl 1 comprises 5 sepals; whorl 2 is composed of the first 10 petals; whorl 3 is composed of stamens in “St Anne's” and petals plus stamens in “Malmaison”; whorl 4 is composed of carpels. Numbers 1 to 5 at the bottom define the flower development stages. Note that “Malmaison” has an enlarged floral receptacle starting from stage 4 (I).
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pone-0009288-g004: Longitudinal sections of floral meristems and flowers during floral organogenesis.(A–J) Sections (stained with toluidine blue) of “Malmaison” (A–D,I) and “St Anne's” (E–H, J) were observed, from the floral meristem stage (stage 1; A, E) until carpel formation (stage 4, I, J). Scale bar equals 150 µm for A to H and 1 mm for I and J. (K) Analysis of floral organogenesis in “Malmaison” (top) and “St Anne's” (bottom). Sepals, petals, stamens and carpels are labeled in yellow, green, blue and red colors, respectively. The different whorls composition is displayed as follows: whorl 1 comprises 5 sepals; whorl 2 is composed of the first 10 petals; whorl 3 is composed of stamens in “St Anne's” and petals plus stamens in “Malmaison”; whorl 4 is composed of carpels. Numbers 1 to 5 at the bottom define the flower development stages. Note that “Malmaison” has an enlarged floral receptacle starting from stage 4 (I).

Mentions: In A. thaliana, floral organ identity is set up during early flower development stages [10]. To identify the stage at which flower size reduction occurs in ‘St Anne's’ as compared to ‘Malmaison’, longitudinal sections of flowers were observed at different flower development stages (Figure 4). First, we divided early flower development in roses into five distinct development stages ranging from the setting of the floral meristem to carpel primordia formation. We interpreted our observations into sketches of longitudinal sections to clearly define the early stages of floral organogenesis (Figure 4K). At stage 1, sepal primordia start to form (presumptive domain in yellow). At stage 2, the first 10 petal primordia (green) emerge. Stage 3 is different in the two genotypes: stamen primordia (in blue) start to form in ‘St Anne's’ while extra petals (in green) appear in ‘Malmaison’. At stage 4, few stamen primordia and carpel primordia (red domain) eventually form in ‘Malmaison’ while only carpel primordia form in ‘St Anne's’. At stage 5, carpels start elongating in both genotypes. To check whether there were differences in meristem size, we measured the flower diameter in sections at different stages of development. The size and shape of floral meristem were similar in ‘Malmaison’ and ‘St Anne's’ flowers at very early stages of floral development (stages 1, 2 and 3; Figure 4A–H), but diverged starting of stage 4. At stage 5, the floral receptacle in ‘St Anne's’ appeared about 20% smaller as compared to ‘Malmaison’. These data show that the difference in total floral organ number between ‘Malmaison’ and ‘St Anne's’ might be due to a difference in floral meristem size starting at floral developmental stage 4 when carpels are forming.


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)

Longitudinal sections of floral meristems and flowers during floral organogenesis.(A–J) Sections (stained with toluidine blue) of “Malmaison” (A–D,I) and “St Anne's” (E–H, J) were observed, from the floral meristem stage (stage 1; A, E) until carpel formation (stage 4, I, J). Scale bar equals 150 µm for A to H and 1 mm for I and J. (K) Analysis of floral organogenesis in “Malmaison” (top) and “St Anne's” (bottom). Sepals, petals, stamens and carpels are labeled in yellow, green, blue and red colors, respectively. The different whorls composition is displayed as follows: whorl 1 comprises 5 sepals; whorl 2 is composed of the first 10 petals; whorl 3 is composed of stamens in “St Anne's” and petals plus stamens in “Malmaison”; whorl 4 is composed of carpels. Numbers 1 to 5 at the bottom define the flower development stages. Note that “Malmaison” has an enlarged floral receptacle starting from stage 4 (I).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2823793&req=5

pone-0009288-g004: Longitudinal sections of floral meristems and flowers during floral organogenesis.(A–J) Sections (stained with toluidine blue) of “Malmaison” (A–D,I) and “St Anne's” (E–H, J) were observed, from the floral meristem stage (stage 1; A, E) until carpel formation (stage 4, I, J). Scale bar equals 150 µm for A to H and 1 mm for I and J. (K) Analysis of floral organogenesis in “Malmaison” (top) and “St Anne's” (bottom). Sepals, petals, stamens and carpels are labeled in yellow, green, blue and red colors, respectively. The different whorls composition is displayed as follows: whorl 1 comprises 5 sepals; whorl 2 is composed of the first 10 petals; whorl 3 is composed of stamens in “St Anne's” and petals plus stamens in “Malmaison”; whorl 4 is composed of carpels. Numbers 1 to 5 at the bottom define the flower development stages. Note that “Malmaison” has an enlarged floral receptacle starting from stage 4 (I).
Mentions: In A. thaliana, floral organ identity is set up during early flower development stages [10]. To identify the stage at which flower size reduction occurs in ‘St Anne's’ as compared to ‘Malmaison’, longitudinal sections of flowers were observed at different flower development stages (Figure 4). First, we divided early flower development in roses into five distinct development stages ranging from the setting of the floral meristem to carpel primordia formation. We interpreted our observations into sketches of longitudinal sections to clearly define the early stages of floral organogenesis (Figure 4K). At stage 1, sepal primordia start to form (presumptive domain in yellow). At stage 2, the first 10 petal primordia (green) emerge. Stage 3 is different in the two genotypes: stamen primordia (in blue) start to form in ‘St Anne's’ while extra petals (in green) appear in ‘Malmaison’. At stage 4, few stamen primordia and carpel primordia (red domain) eventually form in ‘Malmaison’ while only carpel primordia form in ‘St Anne's’. At stage 5, carpels start elongating in both genotypes. To check whether there were differences in meristem size, we measured the flower diameter in sections at different stages of development. The size and shape of floral meristem were similar in ‘Malmaison’ and ‘St Anne's’ flowers at very early stages of floral development (stages 1, 2 and 3; Figure 4A–H), but diverged starting of stage 4. At stage 5, the floral receptacle in ‘St Anne's’ appeared about 20% smaller as compared to ‘Malmaison’. These data show that the difference in total floral organ number between ‘Malmaison’ and ‘St Anne's’ might be due to a difference in floral meristem size starting at floral developmental stage 4 when carpels are forming.

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