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Connecting proline metabolism and signaling pathways in plant senescence.

Zhang L, Becker DF - Front Plant Sci (2015)

Bottom Line: Proline metabolism is manipulated under stress by multiple and complex regulatory pathways and can profoundly influence cell death and survival in microorganisms, plants, and animals.Though the effects of proline are mediated by diverse signaling pathways, a common theme appears to be the generation of reactive oxygen species (ROS) due to proline oxidation being coupled to the respiratory electron transport chain.Future studies focusing on the mechanisms by which proline metabolic shifts occur during senescence may lead to novel methods to rescue crops under stress and to preserve post-harvest agricultural products.

View Article: PubMed Central - PubMed

Affiliation: Redox Biology Center, Department of Biochemistry, University of Nebraska-Lincoln , Lincoln, NE, USA.

ABSTRACT
The amino acid proline has a unique biological role in stress adaptation. Proline metabolism is manipulated under stress by multiple and complex regulatory pathways and can profoundly influence cell death and survival in microorganisms, plants, and animals. Though the effects of proline are mediated by diverse signaling pathways, a common theme appears to be the generation of reactive oxygen species (ROS) due to proline oxidation being coupled to the respiratory electron transport chain. Considerable research has been devoted to understand how plants exploit proline metabolism in response to abiotic and biotic stress. Here, we review potential mechanisms by which proline metabolism influences plant senescence, namely in the petal and leaf. Recent studies of petal senescence suggest proline content is manipulated to meet energy demands of senescing cells. In the flower and leaf, proline metabolism may influence ROS signaling pathways that delay senescence progression. Future studies focusing on the mechanisms by which proline metabolic shifts occur during senescence may lead to novel methods to rescue crops under stress and to preserve post-harvest agricultural products.

No MeSH data available.


Related in: MedlinePlus

Proline metabolic pathways in higher plants. In the biosynthesis pathway, ornithine and glutamate can be converted to glutamate-γ-semialdehyde (GSA) by ornithine-δ-aminotransferase (OAT) and 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), respectively. GSA can then spontaneously cyclize to P5C by losing one molecule of H2O. P5C is the substrate for P5C reductase (P5CR), which catalyzes the last step in proline synthesis. In the catabolic pathway, proline dehydrogenase (PRODH) and P5C dehydrogenase (P5CDH) catalyze the oxidation of proline to glutamate. Electrons from reduced flavin (FADH2) are transferred to the respiratory electron transport chain to regenerate oxidized flavin (FAD) and complete the PRODH catalytic cycle. Glutamate dehydrogenase (GDH) interconverts glutamate and α-ketoglutarate, which enters the tricarboxylic acid cycle. Higher plants harbor two isoforms of P5CS and PRODH.
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Figure 1: Proline metabolic pathways in higher plants. In the biosynthesis pathway, ornithine and glutamate can be converted to glutamate-γ-semialdehyde (GSA) by ornithine-δ-aminotransferase (OAT) and 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), respectively. GSA can then spontaneously cyclize to P5C by losing one molecule of H2O. P5C is the substrate for P5C reductase (P5CR), which catalyzes the last step in proline synthesis. In the catabolic pathway, proline dehydrogenase (PRODH) and P5C dehydrogenase (P5CDH) catalyze the oxidation of proline to glutamate. Electrons from reduced flavin (FADH2) are transferred to the respiratory electron transport chain to regenerate oxidized flavin (FAD) and complete the PRODH catalytic cycle. Glutamate dehydrogenase (GDH) interconverts glutamate and α-ketoglutarate, which enters the tricarboxylic acid cycle. Higher plants harbor two isoforms of P5CS and PRODH.

Mentions: Proline metabolism involves the interconversion of proline and glutamate, a process linked to cellular energetics directly via the respiratory electron transport chain. Proline in higher plants is synthesized from glutamate and ornithine (Fichman et al., 2014). Glutamate-derived proline requires the bifunctional enzyme 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), which catalyzes a two-step reaction requiring ATP and NADPH to generate glutamate-γ-semialdehyde (GSA; Figure 1). GSA spontaneously cyclizes to P5C which is then reduced to proline in a NADPH dependent reaction catalyzed by P5C reductase (P5CR) (P5CR; At5g14800; Liang et al., 2013). In higher plant, P5CS, the rate-limiting enzyme of proline biosynthesis, has two isoforms, P5CS1 (At2g39800) and P5CS2 (At3g55610). P5CS1, localized in the chloroplast, is responsible for stress-induced proline synthesis (Liu et al., 2012a) whereas P5CS2, localized in the cytosol, is important for embryo development (Szekely et al., 2008; Funck et al., 2012). Ornithine-derived proline requires ornithine-δ-aminotransferase, which converts ornithine into GSA (Funck et al., 2008; Fichman et al., 2014).


Connecting proline metabolism and signaling pathways in plant senescence.

Zhang L, Becker DF - Front Plant Sci (2015)

Proline metabolic pathways in higher plants. In the biosynthesis pathway, ornithine and glutamate can be converted to glutamate-γ-semialdehyde (GSA) by ornithine-δ-aminotransferase (OAT) and 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), respectively. GSA can then spontaneously cyclize to P5C by losing one molecule of H2O. P5C is the substrate for P5C reductase (P5CR), which catalyzes the last step in proline synthesis. In the catabolic pathway, proline dehydrogenase (PRODH) and P5C dehydrogenase (P5CDH) catalyze the oxidation of proline to glutamate. Electrons from reduced flavin (FADH2) are transferred to the respiratory electron transport chain to regenerate oxidized flavin (FAD) and complete the PRODH catalytic cycle. Glutamate dehydrogenase (GDH) interconverts glutamate and α-ketoglutarate, which enters the tricarboxylic acid cycle. Higher plants harbor two isoforms of P5CS and PRODH.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4544304&req=5

Figure 1: Proline metabolic pathways in higher plants. In the biosynthesis pathway, ornithine and glutamate can be converted to glutamate-γ-semialdehyde (GSA) by ornithine-δ-aminotransferase (OAT) and 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), respectively. GSA can then spontaneously cyclize to P5C by losing one molecule of H2O. P5C is the substrate for P5C reductase (P5CR), which catalyzes the last step in proline synthesis. In the catabolic pathway, proline dehydrogenase (PRODH) and P5C dehydrogenase (P5CDH) catalyze the oxidation of proline to glutamate. Electrons from reduced flavin (FADH2) are transferred to the respiratory electron transport chain to regenerate oxidized flavin (FAD) and complete the PRODH catalytic cycle. Glutamate dehydrogenase (GDH) interconverts glutamate and α-ketoglutarate, which enters the tricarboxylic acid cycle. Higher plants harbor two isoforms of P5CS and PRODH.
Mentions: Proline metabolism involves the interconversion of proline and glutamate, a process linked to cellular energetics directly via the respiratory electron transport chain. Proline in higher plants is synthesized from glutamate and ornithine (Fichman et al., 2014). Glutamate-derived proline requires the bifunctional enzyme 1Δ-pyrroline-5-carboxylate (P5C) synthetase (P5CS), which catalyzes a two-step reaction requiring ATP and NADPH to generate glutamate-γ-semialdehyde (GSA; Figure 1). GSA spontaneously cyclizes to P5C which is then reduced to proline in a NADPH dependent reaction catalyzed by P5C reductase (P5CR) (P5CR; At5g14800; Liang et al., 2013). In higher plant, P5CS, the rate-limiting enzyme of proline biosynthesis, has two isoforms, P5CS1 (At2g39800) and P5CS2 (At3g55610). P5CS1, localized in the chloroplast, is responsible for stress-induced proline synthesis (Liu et al., 2012a) whereas P5CS2, localized in the cytosol, is important for embryo development (Szekely et al., 2008; Funck et al., 2012). Ornithine-derived proline requires ornithine-δ-aminotransferase, which converts ornithine into GSA (Funck et al., 2008; Fichman et al., 2014).

Bottom Line: Proline metabolism is manipulated under stress by multiple and complex regulatory pathways and can profoundly influence cell death and survival in microorganisms, plants, and animals.Though the effects of proline are mediated by diverse signaling pathways, a common theme appears to be the generation of reactive oxygen species (ROS) due to proline oxidation being coupled to the respiratory electron transport chain.Future studies focusing on the mechanisms by which proline metabolic shifts occur during senescence may lead to novel methods to rescue crops under stress and to preserve post-harvest agricultural products.

View Article: PubMed Central - PubMed

Affiliation: Redox Biology Center, Department of Biochemistry, University of Nebraska-Lincoln , Lincoln, NE, USA.

ABSTRACT
The amino acid proline has a unique biological role in stress adaptation. Proline metabolism is manipulated under stress by multiple and complex regulatory pathways and can profoundly influence cell death and survival in microorganisms, plants, and animals. Though the effects of proline are mediated by diverse signaling pathways, a common theme appears to be the generation of reactive oxygen species (ROS) due to proline oxidation being coupled to the respiratory electron transport chain. Considerable research has been devoted to understand how plants exploit proline metabolism in response to abiotic and biotic stress. Here, we review potential mechanisms by which proline metabolism influences plant senescence, namely in the petal and leaf. Recent studies of petal senescence suggest proline content is manipulated to meet energy demands of senescing cells. In the flower and leaf, proline metabolism may influence ROS signaling pathways that delay senescence progression. Future studies focusing on the mechanisms by which proline metabolic shifts occur during senescence may lead to novel methods to rescue crops under stress and to preserve post-harvest agricultural products.

No MeSH data available.


Related in: MedlinePlus