Limits...
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

Related in: MedlinePlus

Floral organ numbers in “Malmaison” and “St Anne's”.(A) Longitudinal sections of flower in “Malmaison” (left) and in “St Anne's” (right). (B) Floral organs number in “Malmaison” (dark grey) and in “St Anne's” (light grey). Histograms represent the means obtained from 5 flowers from each hybrid. Error bars represent the standard deviation. The two rose varieties differ in two floral characters: organ identity reversions from petals in “Malmaison” to stamens in “St Anne's” and an overall decrease in total organ number. Chimeras: staminoid petals (see Figure S1). (C) Bivariate plot of petal and stamen number showing anti-correlation in “Malmaison” flowers, thus the lability of petal/stamen boundary in this genotype. Each square represents one flower. Correlation and determination coefficients are R = −0.84; R2 = 0.71.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2823793&req=5

pone-0009288-g003: Floral organ numbers in “Malmaison” and “St Anne's”.(A) Longitudinal sections of flower in “Malmaison” (left) and in “St Anne's” (right). (B) Floral organs number in “Malmaison” (dark grey) and in “St Anne's” (light grey). Histograms represent the means obtained from 5 flowers from each hybrid. Error bars represent the standard deviation. The two rose varieties differ in two floral characters: organ identity reversions from petals in “Malmaison” to stamens in “St Anne's” and an overall decrease in total organ number. Chimeras: staminoid petals (see Figure S1). (C) Bivariate plot of petal and stamen number showing anti-correlation in “Malmaison” flowers, thus the lability of petal/stamen boundary in this genotype. Each square represents one flower. Correlation and determination coefficients are R = −0.84; R2 = 0.71.

Mentions: Open flowers were dissected and organs were counted (Figure 3A, B, Table 2 and Figure S1). The total floral organs number was higher in ‘Malmaison’ (about 300) than in ‘St Anne's’ (about 200, Figure 3B). ‘Malmaison’ flowers had five sepals, 97 to 159 petals, 21 to 114 stamens, and 70 to 99 carpels (n = 5, Table 2). The number of stamens negatively correlates with the number of petals (R2 = 0.71) showing that the petal/stamen boundary is labile in ‘Malmaison’ flowers (Figure 3C). Furthermore, except for the outermost ten petals, the rest of ‘Malmaison’ petals were smaller in size compared to those of the ‘St Anne's’ (Figure S1, panels G and H), suggesting that these petals could correspond to transformed stamens. ‘St Anne's’ flowers were composed of 5 sepals, 10 to 15 petals, 123 to 148 stamens and 45 to 63 carpels (n = 5) (Figure 3B; Table 2). In contrast to ‘Malmaison’, the ‘St Anne's’ variety has much lower number of petals, but much higher number of stamens. Staminoid petals were observed in both rose genotypes, but were in a higher proportion in ‘Malmaison’ (Figure 1S panels E and F).


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)

Floral organ numbers in “Malmaison” and “St Anne's”.(A) Longitudinal sections of flower in “Malmaison” (left) and in “St Anne's” (right). (B) Floral organs number in “Malmaison” (dark grey) and in “St Anne's” (light grey). Histograms represent the means obtained from 5 flowers from each hybrid. Error bars represent the standard deviation. The two rose varieties differ in two floral characters: organ identity reversions from petals in “Malmaison” to stamens in “St Anne's” and an overall decrease in total organ number. Chimeras: staminoid petals (see Figure S1). (C) Bivariate plot of petal and stamen number showing anti-correlation in “Malmaison” flowers, thus the lability of petal/stamen boundary in this genotype. Each square represents one flower. Correlation and determination coefficients are R = −0.84; R2 = 0.71.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009288-g003: Floral organ numbers in “Malmaison” and “St Anne's”.(A) Longitudinal sections of flower in “Malmaison” (left) and in “St Anne's” (right). (B) Floral organs number in “Malmaison” (dark grey) and in “St Anne's” (light grey). Histograms represent the means obtained from 5 flowers from each hybrid. Error bars represent the standard deviation. The two rose varieties differ in two floral characters: organ identity reversions from petals in “Malmaison” to stamens in “St Anne's” and an overall decrease in total organ number. Chimeras: staminoid petals (see Figure S1). (C) Bivariate plot of petal and stamen number showing anti-correlation in “Malmaison” flowers, thus the lability of petal/stamen boundary in this genotype. Each square represents one flower. Correlation and determination coefficients are R = −0.84; R2 = 0.71.
Mentions: Open flowers were dissected and organs were counted (Figure 3A, B, Table 2 and Figure S1). The total floral organs number was higher in ‘Malmaison’ (about 300) than in ‘St Anne's’ (about 200, Figure 3B). ‘Malmaison’ flowers had five sepals, 97 to 159 petals, 21 to 114 stamens, and 70 to 99 carpels (n = 5, Table 2). The number of stamens negatively correlates with the number of petals (R2 = 0.71) showing that the petal/stamen boundary is labile in ‘Malmaison’ flowers (Figure 3C). Furthermore, except for the outermost ten petals, the rest of ‘Malmaison’ petals were smaller in size compared to those of the ‘St Anne's’ (Figure S1, panels G and H), suggesting that these petals could correspond to transformed stamens. ‘St Anne's’ flowers were composed of 5 sepals, 10 to 15 petals, 123 to 148 stamens and 45 to 63 carpels (n = 5) (Figure 3B; Table 2). In contrast to ‘Malmaison’, the ‘St Anne's’ variety has much lower number of petals, but much higher number of stamens. Staminoid petals were observed in both rose genotypes, but were in a higher proportion in ‘Malmaison’ (Figure 1S panels E and F).

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
Related in: MedlinePlus