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A Malus crabapple chalcone synthase gene, McCHS, regulates red petal color and flavonoid biosynthesis.

Tai D, Tian J, Zhang J, Song T, Yao Y - PLoS ONE (2014)

Bottom Line: The results showed McCHS have their special expression patterns in each tested cultivars, and is responsible for the red coloration and color variation in crabapple petals, especially for color fade process in 'Radiant'.Furthermore, tobacco plants constitutively expressing McCHS displayed a higher anthocyanins accumulation and a deeper red petal color compared with control untransformed lines.We conclude that the endogenous McCHS gene is a critical factor in the regulation of anthocyanin biosynthesis during petal coloration in Malus crabapple.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Science and Technology, Beijing University of Agriculture, Beijing, China; College of Horticulture, Shanxi Agricultural University, Taigu, Shanxi, China.

ABSTRACT
Chalcone synthase is a key and often rate-limiting enzyme in the biosynthesis of anthocyanin pigments that accumulate in plant organs such as flowers and fruits, but the relationship between CHS expression and the petal coloration level in different cultivars is still unclear. In this study, three typical crabapple cultivars were chosen based on different petal colors and coloration patterns. The two extreme color cultivars, 'Royalty' and 'Flame', have dark red and white petals respectively, while the intermediate cultivar 'Radiant' has pink petals. We detected the flavoniods accumulation and the expression levels of McCHS during petals expansion process in different cultivars. The results showed McCHS have their special expression patterns in each tested cultivars, and is responsible for the red coloration and color variation in crabapple petals, especially for color fade process in 'Radiant'. Furthermore, tobacco plants constitutively expressing McCHS displayed a higher anthocyanins accumulation and a deeper red petal color compared with control untransformed lines. Moreover, the expression levels of several anthocyanin biosynthetic genes were higher in the transgenic McCHS overexpressing tobacco lines than in the control plants. A close relationship was observed between the expression of McCHS and the transcription factors McMYB4 and McMYB5 during petals development in different crabapple cultivars, suggesting that the expression of McCHS was regulated by these transcription factors. We conclude that the endogenous McCHS gene is a critical factor in the regulation of anthocyanin biosynthesis during petal coloration in Malus crabapple.

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Relative expression profile of McCHS in different organs or tissues and chlorophyll content in leaves of the three Malus crabapple cultivars: ‘Royalty’, ‘Radiant’ and ‘Flame’.(A) Relative expression profile of McCHS in different organs or tissues. (B) The Chlorophyll contents in leaves of the three crabapple cultivars. All real time-PCR reactions were normalized using the Ct value corresponding to a Malus crabapple 18S ribosomal RNA gene (DQ341382). Similar material was collected at the same time from the three cultivars. Leaves were all collected at the time of petal stage IV (Figure 2) and the fruits were collected at a fully ripe stage. The Chlorophyll contents of leaves on the tree in vivo were measured by Chlorophyll Content Meter (CL-01, Hansatech, UK). Five Phyllotaxy was measured according to the order of the leaves, respectively. Error bars correspond to the standard error of the mean ± SE of three replicate reactions. Different letters above the bars indicate significantly different values (P<0.05) calculated using one-way analysis of variance (ANOVA) followed by a Duncan's multiple range test.
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pone-0110570-g004: Relative expression profile of McCHS in different organs or tissues and chlorophyll content in leaves of the three Malus crabapple cultivars: ‘Royalty’, ‘Radiant’ and ‘Flame’.(A) Relative expression profile of McCHS in different organs or tissues. (B) The Chlorophyll contents in leaves of the three crabapple cultivars. All real time-PCR reactions were normalized using the Ct value corresponding to a Malus crabapple 18S ribosomal RNA gene (DQ341382). Similar material was collected at the same time from the three cultivars. Leaves were all collected at the time of petal stage IV (Figure 2) and the fruits were collected at a fully ripe stage. The Chlorophyll contents of leaves on the tree in vivo were measured by Chlorophyll Content Meter (CL-01, Hansatech, UK). Five Phyllotaxy was measured according to the order of the leaves, respectively. Error bars correspond to the standard error of the mean ± SE of three replicate reactions. Different letters above the bars indicate significantly different values (P<0.05) calculated using one-way analysis of variance (ANOVA) followed by a Duncan's multiple range test.

Mentions: The expressions of McCHS in leaves and fruits at maturity were also investigated in the three cultivars. The phenotypes of leaf, fruit flesh and fruit pericarp are shown in Figure S1. When comparing leaves, the highest expression of McCHS was in ‘Radiant’, with a value more than twice that of ‘Royalty’ and four times that of ‘Flame’ (Figure 4A). McCHS transcripts were most abundant in the flesh and pericarp of ‘Flame’ fruits, but they were almost undetectable in the pericarp of ‘Royalty’ and ‘Radiant’ (Figure 4A). In fruit flesh, the expression profile of McCHS showed an opposite trend from that of leaves (Figure 4A). These results suggest that the expression of McCHS have different patterns in different tissues/organs among these three cultivars, so we deduced that the expression of McCHS may be also involved in other flavonoids compounds biosynthesis. As an important factor to determine the leaf color, the chlorophyll contents in leaves from the three cultivars were measured at five development stages, the results suggested that the chlorophyll content was higher in ever-red-leaf ‘Royalty’ leaves than spring-red-leaf ‘Radiant’ and ever-green-leaf ‘Flame’, and gradually decreased with the development of leaves in crabapple. So the red leaf color of crabapple is depended on the accumulation of anthocyanin and expression of McCHS, not the chlorophyll content (Figure 4B).


A Malus crabapple chalcone synthase gene, McCHS, regulates red petal color and flavonoid biosynthesis.

Tai D, Tian J, Zhang J, Song T, Yao Y - PLoS ONE (2014)

Relative expression profile of McCHS in different organs or tissues and chlorophyll content in leaves of the three Malus crabapple cultivars: ‘Royalty’, ‘Radiant’ and ‘Flame’.(A) Relative expression profile of McCHS in different organs or tissues. (B) The Chlorophyll contents in leaves of the three crabapple cultivars. All real time-PCR reactions were normalized using the Ct value corresponding to a Malus crabapple 18S ribosomal RNA gene (DQ341382). Similar material was collected at the same time from the three cultivars. Leaves were all collected at the time of petal stage IV (Figure 2) and the fruits were collected at a fully ripe stage. The Chlorophyll contents of leaves on the tree in vivo were measured by Chlorophyll Content Meter (CL-01, Hansatech, UK). Five Phyllotaxy was measured according to the order of the leaves, respectively. Error bars correspond to the standard error of the mean ± SE of three replicate reactions. Different letters above the bars indicate significantly different values (P<0.05) calculated using one-way analysis of variance (ANOVA) followed by a Duncan's multiple range test.
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pone-0110570-g004: Relative expression profile of McCHS in different organs or tissues and chlorophyll content in leaves of the three Malus crabapple cultivars: ‘Royalty’, ‘Radiant’ and ‘Flame’.(A) Relative expression profile of McCHS in different organs or tissues. (B) The Chlorophyll contents in leaves of the three crabapple cultivars. All real time-PCR reactions were normalized using the Ct value corresponding to a Malus crabapple 18S ribosomal RNA gene (DQ341382). Similar material was collected at the same time from the three cultivars. Leaves were all collected at the time of petal stage IV (Figure 2) and the fruits were collected at a fully ripe stage. The Chlorophyll contents of leaves on the tree in vivo were measured by Chlorophyll Content Meter (CL-01, Hansatech, UK). Five Phyllotaxy was measured according to the order of the leaves, respectively. Error bars correspond to the standard error of the mean ± SE of three replicate reactions. Different letters above the bars indicate significantly different values (P<0.05) calculated using one-way analysis of variance (ANOVA) followed by a Duncan's multiple range test.
Mentions: The expressions of McCHS in leaves and fruits at maturity were also investigated in the three cultivars. The phenotypes of leaf, fruit flesh and fruit pericarp are shown in Figure S1. When comparing leaves, the highest expression of McCHS was in ‘Radiant’, with a value more than twice that of ‘Royalty’ and four times that of ‘Flame’ (Figure 4A). McCHS transcripts were most abundant in the flesh and pericarp of ‘Flame’ fruits, but they were almost undetectable in the pericarp of ‘Royalty’ and ‘Radiant’ (Figure 4A). In fruit flesh, the expression profile of McCHS showed an opposite trend from that of leaves (Figure 4A). These results suggest that the expression of McCHS have different patterns in different tissues/organs among these three cultivars, so we deduced that the expression of McCHS may be also involved in other flavonoids compounds biosynthesis. As an important factor to determine the leaf color, the chlorophyll contents in leaves from the three cultivars were measured at five development stages, the results suggested that the chlorophyll content was higher in ever-red-leaf ‘Royalty’ leaves than spring-red-leaf ‘Radiant’ and ever-green-leaf ‘Flame’, and gradually decreased with the development of leaves in crabapple. So the red leaf color of crabapple is depended on the accumulation of anthocyanin and expression of McCHS, not the chlorophyll content (Figure 4B).

Bottom Line: The results showed McCHS have their special expression patterns in each tested cultivars, and is responsible for the red coloration and color variation in crabapple petals, especially for color fade process in 'Radiant'.Furthermore, tobacco plants constitutively expressing McCHS displayed a higher anthocyanins accumulation and a deeper red petal color compared with control untransformed lines.We conclude that the endogenous McCHS gene is a critical factor in the regulation of anthocyanin biosynthesis during petal coloration in Malus crabapple.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Science and Technology, Beijing University of Agriculture, Beijing, China; College of Horticulture, Shanxi Agricultural University, Taigu, Shanxi, China.

ABSTRACT
Chalcone synthase is a key and often rate-limiting enzyme in the biosynthesis of anthocyanin pigments that accumulate in plant organs such as flowers and fruits, but the relationship between CHS expression and the petal coloration level in different cultivars is still unclear. In this study, three typical crabapple cultivars were chosen based on different petal colors and coloration patterns. The two extreme color cultivars, 'Royalty' and 'Flame', have dark red and white petals respectively, while the intermediate cultivar 'Radiant' has pink petals. We detected the flavoniods accumulation and the expression levels of McCHS during petals expansion process in different cultivars. The results showed McCHS have their special expression patterns in each tested cultivars, and is responsible for the red coloration and color variation in crabapple petals, especially for color fade process in 'Radiant'. Furthermore, tobacco plants constitutively expressing McCHS displayed a higher anthocyanins accumulation and a deeper red petal color compared with control untransformed lines. Moreover, the expression levels of several anthocyanin biosynthetic genes were higher in the transgenic McCHS overexpressing tobacco lines than in the control plants. A close relationship was observed between the expression of McCHS and the transcription factors McMYB4 and McMYB5 during petals development in different crabapple cultivars, suggesting that the expression of McCHS was regulated by these transcription factors. We conclude that the endogenous McCHS gene is a critical factor in the regulation of anthocyanin biosynthesis during petal coloration in Malus crabapple.

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