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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
‘Malmaison’ and ‘St Anne's’ rose varieties display highly similar phenotypes, except for floral architecture.(A) Contrasting floral morphologies of R. x hybrida ‘Malmaison’ (double flower, left) and its genetically related variety R. x hybrida ‘St Anne's’ (semi-double flower, right). (B) Morphometric analysis of leaves. The photo displays a rose leaf and the 32 landmarks (red dots) that were used for measurements. No significant difference could be observed in leaf morphology between the two rose hybrids. (C) Gas Chromatography-Flame Ionization Detector (GC-FID) analysis on solid/liquid extracts of petals and stamens of R. x hybrida ‘St Anne's’ and ‘Malmaison’, showing that individually, the floral organs (petals and stamens) produce similar volatile compounds in both cultivars.
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pone-0009288-g002: ‘Malmaison’ and ‘St Anne's’ rose varieties display highly similar phenotypes, except for floral architecture.(A) Contrasting floral morphologies of R. x hybrida ‘Malmaison’ (double flower, left) and its genetically related variety R. x hybrida ‘St Anne's’ (semi-double flower, right). (B) Morphometric analysis of leaves. The photo displays a rose leaf and the 32 landmarks (red dots) that were used for measurements. No significant difference could be observed in leaf morphology between the two rose hybrids. (C) Gas Chromatography-Flame Ionization Detector (GC-FID) analysis on solid/liquid extracts of petals and stamens of R. x hybrida ‘St Anne's’ and ‘Malmaison’, showing that individually, the floral organs (petals and stamens) produce similar volatile compounds in both cultivars.

Mentions: Sport cultivars, i.e. spontaneous somatic mutants, represent an interesting resource for breeders, as well as for molecular studies. It is estimated that up to 10% of cultivated rose varieties [17] are sport cultivars and they are widely used to generate new cultivars. R. x hybrida ‘Souvenir de la Malmaison’ (‘Malmaison’ hereafter) is a triploid hybrid originating from crosses between European and Chinese rose gene pools [8]. As these crosses occurred in the ‘Réunion’ (originally named ‘Bourbon’) Island, the resulting generation of triploid hybrids was designated as ‘Bourbon’ roses. ‘Malmaison’ has double flowers comprising over 100 petals (Figure 2A). R. x hybrida ‘Souvenir de St Anne's’ (‘St Anne's’ hereafter) is a bud-sport cultivar of ‘Malmaison’ [17]. ‘St Anne's’ cultivar has semi-double flowers with a much lower (about 10) petal number (Figure 2A). Although their floral phenotypes are conspicuously different, historical records indicate that ‘St Anne's’ derives from ‘Malmaison’ by spontaneous mutation and thus they should be nearly isogenic [17]. We confirmed that ‘St Anne's’ is a true sport of ‘Malmaison’ using four different ISSR primers that revealed identical amplification patterns between ‘Malmaison’ and ‘St Anne's’ (data not shown). Then, we examined the vegetative organ morphology and secondary metabolism activity in these two rose varieties. Both roses show similar vegetative growth patterns. Leaf morphology in ‘Malmaison’ and ‘St Anne's’ individuals was analyzed using the AAM Toolbox [18]. Thirty-two morphological measurements were obtained for each leaf (including leaflet area, length and width, petiole, rachis and petiolule length) and compared between hybrids (Figure 2B). The size and shape of all analyzed leaves from ‘Malmaison’ and ‘St Anne's’ show little variation, suggesting that both hybrids have very similar vegetative growth. We next investigated the scent composition of ‘Malmaison’ and ‘St Anne's’ since even closely related varieties can have very different fragrances [19]. Flowers of both ‘Malmaison’ and ‘St Anne's’ are heavily scented, but have slightly different scent. We conducted a headspace scent analysis and confirmed that some compounds like eugenol and methyleugenol, which give a clove scent, were present only in the headspace of ‘St Anne's’ (Table 1). We then analyzed the volatiles separately in petals and stamens by solvent extraction followed by gas chromatography. The stamens from both ‘Malmaison’ and ‘St Anne's’ produced predominantly eugenol and the petals produced mainly 2-phenylethanol, a major floral scent compound (Figure 2C). Scent signatures from both rose cultivars were identical in petals and showed only slight differences in stamens, suggesting that the mutations resulted in the ‘St Anne's’ variety only affected organ number and identity, but likely not scent. The fact that a clove scent was perceptible in ‘St Anne's’ is most probably due to the larger number of stamens in this particular variety.


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)

‘Malmaison’ and ‘St Anne's’ rose varieties display highly similar phenotypes, except for floral architecture.(A) Contrasting floral morphologies of R. x hybrida ‘Malmaison’ (double flower, left) and its genetically related variety R. x hybrida ‘St Anne's’ (semi-double flower, right). (B) Morphometric analysis of leaves. The photo displays a rose leaf and the 32 landmarks (red dots) that were used for measurements. No significant difference could be observed in leaf morphology between the two rose hybrids. (C) Gas Chromatography-Flame Ionization Detector (GC-FID) analysis on solid/liquid extracts of petals and stamens of R. x hybrida ‘St Anne's’ and ‘Malmaison’, showing that individually, the floral organs (petals and stamens) produce similar volatile compounds in both cultivars.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0009288-g002: ‘Malmaison’ and ‘St Anne's’ rose varieties display highly similar phenotypes, except for floral architecture.(A) Contrasting floral morphologies of R. x hybrida ‘Malmaison’ (double flower, left) and its genetically related variety R. x hybrida ‘St Anne's’ (semi-double flower, right). (B) Morphometric analysis of leaves. The photo displays a rose leaf and the 32 landmarks (red dots) that were used for measurements. No significant difference could be observed in leaf morphology between the two rose hybrids. (C) Gas Chromatography-Flame Ionization Detector (GC-FID) analysis on solid/liquid extracts of petals and stamens of R. x hybrida ‘St Anne's’ and ‘Malmaison’, showing that individually, the floral organs (petals and stamens) produce similar volatile compounds in both cultivars.
Mentions: Sport cultivars, i.e. spontaneous somatic mutants, represent an interesting resource for breeders, as well as for molecular studies. It is estimated that up to 10% of cultivated rose varieties [17] are sport cultivars and they are widely used to generate new cultivars. R. x hybrida ‘Souvenir de la Malmaison’ (‘Malmaison’ hereafter) is a triploid hybrid originating from crosses between European and Chinese rose gene pools [8]. As these crosses occurred in the ‘Réunion’ (originally named ‘Bourbon’) Island, the resulting generation of triploid hybrids was designated as ‘Bourbon’ roses. ‘Malmaison’ has double flowers comprising over 100 petals (Figure 2A). R. x hybrida ‘Souvenir de St Anne's’ (‘St Anne's’ hereafter) is a bud-sport cultivar of ‘Malmaison’ [17]. ‘St Anne's’ cultivar has semi-double flowers with a much lower (about 10) petal number (Figure 2A). Although their floral phenotypes are conspicuously different, historical records indicate that ‘St Anne's’ derives from ‘Malmaison’ by spontaneous mutation and thus they should be nearly isogenic [17]. We confirmed that ‘St Anne's’ is a true sport of ‘Malmaison’ using four different ISSR primers that revealed identical amplification patterns between ‘Malmaison’ and ‘St Anne's’ (data not shown). Then, we examined the vegetative organ morphology and secondary metabolism activity in these two rose varieties. Both roses show similar vegetative growth patterns. Leaf morphology in ‘Malmaison’ and ‘St Anne's’ individuals was analyzed using the AAM Toolbox [18]. Thirty-two morphological measurements were obtained for each leaf (including leaflet area, length and width, petiole, rachis and petiolule length) and compared between hybrids (Figure 2B). The size and shape of all analyzed leaves from ‘Malmaison’ and ‘St Anne's’ show little variation, suggesting that both hybrids have very similar vegetative growth. We next investigated the scent composition of ‘Malmaison’ and ‘St Anne's’ since even closely related varieties can have very different fragrances [19]. Flowers of both ‘Malmaison’ and ‘St Anne's’ are heavily scented, but have slightly different scent. We conducted a headspace scent analysis and confirmed that some compounds like eugenol and methyleugenol, which give a clove scent, were present only in the headspace of ‘St Anne's’ (Table 1). We then analyzed the volatiles separately in petals and stamens by solvent extraction followed by gas chromatography. The stamens from both ‘Malmaison’ and ‘St Anne's’ produced predominantly eugenol and the petals produced mainly 2-phenylethanol, a major floral scent compound (Figure 2C). Scent signatures from both rose cultivars were identical in petals and showed only slight differences in stamens, suggesting that the mutations resulted in the ‘St Anne's’ variety only affected organ number and identity, but likely not scent. The fact that a clove scent was perceptible in ‘St Anne's’ is most probably due to the larger number of stamens in this particular variety.

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