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The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates.

Casañal A, Zander U, Muñoz C, Dupeux F, Luque I, Botella MA, Schwab W, Valpuesta V, Marquez JA - J. Biol. Chem. (2013)

Bottom Line: Recently, three new members of the PR-10 family, the Fra a proteins, have been identified in strawberry, where they are required for the activity of the flavonoid biosynthesis pathway, which is essential for the development of color and flavor in fruits.Here, we show that Fra a proteins bind natural flavonoids with different selectivity and affinities in the low μm range.Our findings provide mechanistic insight on the function of Fra a proteins and suggest that PR-10 proteins, which are widespread in plants, may play a role in the control of secondary metabolic pathways by binding to metabolic intermediates.

View Article: PubMed Central - PubMed

Affiliation: From the Instituto de Hortofruticultura Subtropical y Mediterránea (IHSM-UMA-Consejo Superior de Investigaciones Científicas), Departamento de Biología Molecular y Bioquímica, Universidad de Málaga, 29071 Málaga, Spain.

ABSTRACT
Pathogenesis-related 10 (PR-10) proteins are involved in many aspects of plant biology but their molecular function is still unclear. They are related by sequence and structural homology to mammalian lipid transport and plant abscisic acid receptor proteins and are predicted to have cavities for ligand binding. Recently, three new members of the PR-10 family, the Fra a proteins, have been identified in strawberry, where they are required for the activity of the flavonoid biosynthesis pathway, which is essential for the development of color and flavor in fruits. Here, we show that Fra a proteins bind natural flavonoids with different selectivity and affinities in the low μm range. The structural analysis of Fra a 1 E and a Fra a 3-catechin complex indicates that loops L3, L5, and L7 surrounding the ligand-binding cavity show significant flexibility in the apo forms but close over the ligand in the Fra a 3-catechin complex. Our findings provide mechanistic insight on the function of Fra a proteins and suggest that PR-10 proteins, which are widespread in plants, may play a role in the control of secondary metabolic pathways by binding to metabolic intermediates.

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Related in: MedlinePlus

The phenolic compound biosynthesis pathway. A schematic representation of the phenylpropanoid and flavonoid biosynthesis pathway is shown. Major families of flavonoid compounds are highlighted. Flavonoids are characterized by the presence of the flavan nucleus with A, B, and C rings as indicated (inset). Final products of the flavonoid pathway such as pelargonidin 3-O-glucoside, are often glycosylated at the position 3 of the C ring of the flavan nucleus. Suppression of Fra a protein expression affects the expression of phenylalanine ammonia lyase (PAL) and chalcone synthase (CHS) genes (red inverted triangles) and alters phenolic compound accumulation with an increase in the levels of catechin and a decreased accumulation of anthocyanins (as indicated by arrows) (28).
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Figure 1: The phenolic compound biosynthesis pathway. A schematic representation of the phenylpropanoid and flavonoid biosynthesis pathway is shown. Major families of flavonoid compounds are highlighted. Flavonoids are characterized by the presence of the flavan nucleus with A, B, and C rings as indicated (inset). Final products of the flavonoid pathway such as pelargonidin 3-O-glucoside, are often glycosylated at the position 3 of the C ring of the flavan nucleus. Suppression of Fra a protein expression affects the expression of phenylalanine ammonia lyase (PAL) and chalcone synthase (CHS) genes (red inverted triangles) and alters phenolic compound accumulation with an increase in the levels of catechin and a decreased accumulation of anthocyanins (as indicated by arrows) (28).

Mentions: Flavonoids and phenolic compounds are among the most important secondary metabolites in plants. In addition to color and flavor development, they participate in many aspects of plant biology, including UV protection, as antioxidants, auxin transport regulators, and defense compounds against pathogens (29–33). Thus, injury by pathogens or pests induces the accumulation of flavonoids and other phenolic compounds with antimicrobial activity (34). Flavonoids are also exuded by plant roots and act as signals that modify the transcriptional activity of nodulation genes in nitrogen-fixing bacteria, thereby promoting symbiotic association (35, 36). Other flavonoids have been implicated in pollen germination, seed resistance to pests and numerous other processes (36, 37). The effect of dietary flavonoids in human health is also a subject of study due to their antioxidative and anticarcinogenic activities (38). Flavonoids are synthesized via the phenylpropanoid and flavonoid pathways (see Fig. 1) (30, 32). The first step in the phenylpropanoid pathway is catalyzed by the enzyme phenylalanine ammonia-lyase (PAL) and leads to the production of cinnamic acid from l-phenylalanine. PAL is the gateway enzyme to the synthesis of phenolic and flavonoid compounds as well as many other secondary metabolites (32). In Arabidopsis and other species, PAL gene expression is responsive to developmental and environmental clues such as wounding, pathogen infection, or UV radiation, among others (39–43). Another important step in the synthesis of flavonoids is the production of naringenin, which is the first product in the pathway with a flavan structure and from which many other flavonoids are derived (see Fig. 1). This step is catalyzed by the enzyme chalcone synthase. Many of the final products of the flavonoid biosynthesis pathway accumulate as O-glycosyl derivatives at the position 3 of the C ring of the flavan nucleus and are accumulated in the vacuole or secreted through the plasma membrane into the apoplastic space (44). A number of flavonoids that account for color of the fruit and contribute significantly to its taste are produced in the strawberry fruit in a developmental-specific pattern (29, 45). Proanthocyanidins (condensed tannins) are mostly produced in the young fruits that make them bitter, whereas anthocyanins, mostly pelargonidin-3-O-glucoside and cyanidin-3-O-glucoside (see Fig. 1), which confer color, are abundant in the later stages of fruit maturation.


The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates.

Casañal A, Zander U, Muñoz C, Dupeux F, Luque I, Botella MA, Schwab W, Valpuesta V, Marquez JA - J. Biol. Chem. (2013)

The phenolic compound biosynthesis pathway. A schematic representation of the phenylpropanoid and flavonoid biosynthesis pathway is shown. Major families of flavonoid compounds are highlighted. Flavonoids are characterized by the presence of the flavan nucleus with A, B, and C rings as indicated (inset). Final products of the flavonoid pathway such as pelargonidin 3-O-glucoside, are often glycosylated at the position 3 of the C ring of the flavan nucleus. Suppression of Fra a protein expression affects the expression of phenylalanine ammonia lyase (PAL) and chalcone synthase (CHS) genes (red inverted triangles) and alters phenolic compound accumulation with an increase in the levels of catechin and a decreased accumulation of anthocyanins (as indicated by arrows) (28).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3853281&req=5

Figure 1: The phenolic compound biosynthesis pathway. A schematic representation of the phenylpropanoid and flavonoid biosynthesis pathway is shown. Major families of flavonoid compounds are highlighted. Flavonoids are characterized by the presence of the flavan nucleus with A, B, and C rings as indicated (inset). Final products of the flavonoid pathway such as pelargonidin 3-O-glucoside, are often glycosylated at the position 3 of the C ring of the flavan nucleus. Suppression of Fra a protein expression affects the expression of phenylalanine ammonia lyase (PAL) and chalcone synthase (CHS) genes (red inverted triangles) and alters phenolic compound accumulation with an increase in the levels of catechin and a decreased accumulation of anthocyanins (as indicated by arrows) (28).
Mentions: Flavonoids and phenolic compounds are among the most important secondary metabolites in plants. In addition to color and flavor development, they participate in many aspects of plant biology, including UV protection, as antioxidants, auxin transport regulators, and defense compounds against pathogens (29–33). Thus, injury by pathogens or pests induces the accumulation of flavonoids and other phenolic compounds with antimicrobial activity (34). Flavonoids are also exuded by plant roots and act as signals that modify the transcriptional activity of nodulation genes in nitrogen-fixing bacteria, thereby promoting symbiotic association (35, 36). Other flavonoids have been implicated in pollen germination, seed resistance to pests and numerous other processes (36, 37). The effect of dietary flavonoids in human health is also a subject of study due to their antioxidative and anticarcinogenic activities (38). Flavonoids are synthesized via the phenylpropanoid and flavonoid pathways (see Fig. 1) (30, 32). The first step in the phenylpropanoid pathway is catalyzed by the enzyme phenylalanine ammonia-lyase (PAL) and leads to the production of cinnamic acid from l-phenylalanine. PAL is the gateway enzyme to the synthesis of phenolic and flavonoid compounds as well as many other secondary metabolites (32). In Arabidopsis and other species, PAL gene expression is responsive to developmental and environmental clues such as wounding, pathogen infection, or UV radiation, among others (39–43). Another important step in the synthesis of flavonoids is the production of naringenin, which is the first product in the pathway with a flavan structure and from which many other flavonoids are derived (see Fig. 1). This step is catalyzed by the enzyme chalcone synthase. Many of the final products of the flavonoid biosynthesis pathway accumulate as O-glycosyl derivatives at the position 3 of the C ring of the flavan nucleus and are accumulated in the vacuole or secreted through the plasma membrane into the apoplastic space (44). A number of flavonoids that account for color of the fruit and contribute significantly to its taste are produced in the strawberry fruit in a developmental-specific pattern (29, 45). Proanthocyanidins (condensed tannins) are mostly produced in the young fruits that make them bitter, whereas anthocyanins, mostly pelargonidin-3-O-glucoside and cyanidin-3-O-glucoside (see Fig. 1), which confer color, are abundant in the later stages of fruit maturation.

Bottom Line: Recently, three new members of the PR-10 family, the Fra a proteins, have been identified in strawberry, where they are required for the activity of the flavonoid biosynthesis pathway, which is essential for the development of color and flavor in fruits.Here, we show that Fra a proteins bind natural flavonoids with different selectivity and affinities in the low μm range.Our findings provide mechanistic insight on the function of Fra a proteins and suggest that PR-10 proteins, which are widespread in plants, may play a role in the control of secondary metabolic pathways by binding to metabolic intermediates.

View Article: PubMed Central - PubMed

Affiliation: From the Instituto de Hortofruticultura Subtropical y Mediterránea (IHSM-UMA-Consejo Superior de Investigaciones Científicas), Departamento de Biología Molecular y Bioquímica, Universidad de Málaga, 29071 Málaga, Spain.

ABSTRACT
Pathogenesis-related 10 (PR-10) proteins are involved in many aspects of plant biology but their molecular function is still unclear. They are related by sequence and structural homology to mammalian lipid transport and plant abscisic acid receptor proteins and are predicted to have cavities for ligand binding. Recently, three new members of the PR-10 family, the Fra a proteins, have been identified in strawberry, where they are required for the activity of the flavonoid biosynthesis pathway, which is essential for the development of color and flavor in fruits. Here, we show that Fra a proteins bind natural flavonoids with different selectivity and affinities in the low μm range. The structural analysis of Fra a 1 E and a Fra a 3-catechin complex indicates that loops L3, L5, and L7 surrounding the ligand-binding cavity show significant flexibility in the apo forms but close over the ligand in the Fra a 3-catechin complex. Our findings provide mechanistic insight on the function of Fra a proteins and suggest that PR-10 proteins, which are widespread in plants, may play a role in the control of secondary metabolic pathways by binding to metabolic intermediates.

Show MeSH
Related in: MedlinePlus