Proline: a multifunctional amino acid

doi:10.1016/j.tplants.2009.11.009

Trends in Plant Science

Volume 15, Issue 2, February 2010, Pages 89-97

https://doi.org/10.1016/j.tplants.2009.11.009 Get rights and content

Proline accumulates in many plant species in response to environmental stress. Although much is now known about proline metabolism, some aspects of its biological functions are still unclear. Here, we discuss the compartmentalization of proline biosynthesis, accumulation and degradation in the cytosol, chloroplast and mitochondria. We also describe the role of proline in cellular homeostasis, including redox balance and energy status. Proline can act as a signaling molecule to modulate mitochondrial functions, influence cell proliferation or cell death and trigger specific gene expression, which can be essential for plant recovery from stress. Although the regulation and function of proline accumulation are not yet completely understood, the engineering of proline metabolism could lead to new opportunities to improve plant tolerance of environmental stresses.

Section snippets

Proline accumulation in plants

Proline is a proteinogenic amino acid with an exceptional conformational rigidity, and is essential for primary metabolism. Since the first report on proline accumulation in wilting perennial rye grass (Lolium perenne) [1], numerous studies have shown that the proline content in higher plants increases under different environmental stresses. Proline accumulation has been reported during conditions of drought [2] high salinity [3] high light and UV irradiation [4], heavy metals [5], oxidative

Compartmentalization of proline metabolism in plants

In plants, proline is synthesized mainly from glutamate, which is reduced to glutamate-semialdehyde (GSA) by the pyrroline-5-carboxylate synthetase (P5CS) enzyme, and spontaneously converted to pyrroline-5-carboxylate (P5C) 22, 23 (Figure 1). P5C reductase (P5CR) further reduces the P5C intermediate to proline 24, 25. In most plant species, P5CS is encoded by two genes and P5CR is encoded by one 25, 26, 27. Proline catabolism occurs in mitochondria via the sequential action of proline

Regulation of proline metabolism

Although proline metabolism has been studied for >40 years in plants, little is known about the signaling pathways involved in its regulation. Proline biosynthesis is activated and its catabolism repressed during dehydration, whereas rehydration triggers the opposite regulation 3, 26, 28, 29, 30, 39 (Figure 2). Proline biosynthesis is controlled by the activity of two P5CS genes in plants, encoding one housekeeping and one stress-specific P5CS isoform. Although the duplicated P5CS genes share a

Proline accumulation and stress tolerance

For a long time, proline was considered as an inert compatible osmolyte that protects subcellular structures and macromolecules under osmotic stress 10, 11, 12. However, proline accumulation can influence stress tolerance in multiple ways (Figure 3). Proline has been shown to function as a molecular chaperone able to protect protein integrity and enhance the activities of different enzymes. Examples of such roles include the prevention of protein aggregation and stabilization of M4 lactate

Regulatory functions of proline

Increasing amounts of data suggest that proline has certain regulatory functions, controls plant development and acts as a signal molecule. Antisense expression of P5CS1 in transgenic Arabidopsis led to proline depletion and resulted in abnormal leaf morphology and defective inflorescences [90]. A p5cs2-knockout mutant displays embryo lethality and proline-rescued mutant plants show aberrant growth, implying that an adequate proline supply is essential for embryo and plant development [20].

Concluding remarks and perspectives

Although proline has long been considered as a compatible osmolyte, recent results highlight its multiple functions in stress adaptation, recovery and signaling. Compartmentalization of proline biosynthesis and degradation in the cytosol, chloroplast and mitochondria add to the complexity of functional diversification of proline metabolism. Stabilization of proteins and protein complexes in the chloroplast and cytosol, protection of the photosynthetic apparatus and enzymes involved in

Acknowledgements

Aviah Zilberstein, Csaba Koncz and members of the Savouré laboratory are gratefully acknowledged for their stimulating discussions and comments on the article. Research and preparation of the paper was supported by the OTKA grant No. K68226, NKFP grant No.4-038-04, the COST program No. FA0605 and the bilateral French-Hungarian (Balaton) collaboration program FR34/2008. The authors also thank four anonymous reviewers for their valuable comments and input.

References (109)

P.P. Saradhi
Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation
Biochem. Biophys. Res. Commun.
(1995)
S.L. Yang
Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings
J. Plant Physiol.
(2009)
L.N. Csonka
Nucleotide sequence of a mutation in the proB gene of Escherichia coli that confers proline overproduction and enhanced tolerance to osmotic stress
Gene
(1988)
G. Miller
Unraveling delta1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes
J. Biol. Chem.
(2009)
A. Savouré
Isolation, characterization, and chromosomal location of a gene encoding the delta 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana
FEBS Lett.
(1995)
A.J. Delauney
Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis
J. Biol. Chem.
(1993)
T. Kleffmann
The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions
Curr. Biol.
(2004)
C. Yu
Transport of glycine, serine, and proline into spinach leaf mitochondria
Arch. Biochem. Biophys.
(1983)
L. Palmieri
Arabidopsis mitochondria have two basic amino acid transporters with partially overlapping specificities and differential expression in seedling development
Biochim. Biophys. Acta
(2006)
L. Thiery
Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis thaliana
J. Biol. Chem.
(2004)

J.H. Yoo

Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis

J. Biol. Chem.

(2005)

C.S. Zhang

Removal of feedback inhibition of delta 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalysing the first two steps of proline biosynthesis in plants

J. Biol. Chem.

(1995)

X. Hua

A 69 bp fragment in the pyrroline-5-carboxylate reductase promoter of Arabidopsis thaliana activates minimal CaMV 35S promoter in a tissue-specific manner

FEBS Lett.

(1999)

O. Borsani

Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis

Cell

(2005)

C.S. Rajendrakumar

Proline-protein interactions: protection of structural and functional integrity of M4 lactate dehydrogenase

Biochem. Biophys. Res. Commun.

(1994)

P. Sharma et al.

Modulation of nitrate reductase activity in rice seedlings under aluminium toxicity and water stress: role of osmolytes as enzyme protectant

J Plant Physiol.

(2005)

S. Mishra et al.

Inhibition of ribonuclease and protease activities in arsenic exposed rice seedlings: role of proline as enzyme protectant

J Plant Physiol.

(2006)

N. Smirnoff et al.

Hydroxyl radical scavenging activity of compatible solutes

Phytochemistry

(1989)

N. Krishnan

Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress

Free Radical Biol. Med.

(2008)

M.A. Hoque

Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells

J. Plant Physiol.

(2008)

M.M. Islam

Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells

J. Plant Physiol.

(2009)

J.A. De Ronde

Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress

J Plant Physiol.

(2004)

E.P. Murakeozy

Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary

J. Plant Physiol.

(2003)

A.R. Kemble et al.

Liberation of amino acids in perennial ray grass during wilting

Biochem. J.

(1954)

N.L. Choudhary

Expression of delta1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.)

Ind. J. Biochem. Biophys.

(2005)

Y. Yoshiba

Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress

Plant J.

(1995)

H. Schat

Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris

Physiol. Plant.

(1997)

G. Fabro

Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis

Mol. Plant–Microbe Interact.

(2004)

E. Haudecoeur

Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens

Proc. Natl. Acad. Sci. U. S. A.

(2009)

L.N. Csonka et al.

Prokaryotic osmoregulation: genetics and physiology

Annu. Rev. Microbiol.

(1991)

P. Hare et al.

Metabolic implications of stress induced proline accumulation in plants

Plant Growth Regul.

(1997)

P.B. Kavi Kishor

Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance

Curr. Sci.

(2005)

N. Verbruggen et al.

Proline accumulation in plants: a review

Amino Acids

(2008)

J. Liu et al.

Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis

Plant Physiol.

(1997)

Z. Xin et al.

Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant

Proc. Natl. Acad. Sci. U. S. A.

(1998)

Z. Chen

Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance

J. Exp. Bot.

(2007)

Widodo

Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance

J. Exp. Bot.

(2009)

Z. Hong

Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress

Plant Physiol.

(2000)

R. Mattioli

Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis

Plant Mol. Biol.

(2008)

G. Székely

Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis

Plant J.

(2008)

C.A. Hu

A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyses the first two steps in proline biosynthesis in plants

Proc. Natl. Acad. Sci. U. S. A.

(1992)

A. Szoke

Subcellular location of delta-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean

Plant Physiol.

(1992)

N. Verbruggen

Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana

Plant Physiol.

(1993)

N. Strizhov

Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis

Plant J

(1997)

P. Armengaud

Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features

Physiol. Plant

(2004)

T. Kiyosue

A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis

Plant Cell

(1996)

N. Verbruggen

Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator

Proc. Natl. Acad. Sci. U. S. A.

(1996)

K. Deuschle

A nuclear gene encoding mitochondrial Delta-pyrroline-5-carboxylate dehydrogenase and its potential role in protection from proline toxicity

Plant J.

(2001)

A. Ribarits

Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development

Planta

(2007)

N.H. Roosens

Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana

Plant Physiol.

(1998)

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Trends in Plant Science

ReviewProline: a multifunctional amino acid

Section snippets

Proline accumulation in plants

Compartmentalization of proline metabolism in plants

Regulation of proline metabolism

Proline accumulation and stress tolerance

Regulatory functions of proline

Concluding remarks and perspectives

Acknowledgements

Biochem. Biophys. Res. Commun.

J. Plant Physiol.

Gene

J. Biol. Chem.

FEBS Lett.

J. Biol. Chem.

Curr. Biol.

Arch. Biochem. Biophys.

Biochim. Biophys. Acta

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

FEBS Lett.

Cell

Biochem. Biophys. Res. Commun.

J Plant Physiol.

J Plant Physiol.

Phytochemistry

Free Radical Biol. Med.

J. Plant Physiol.

J. Plant Physiol.

J Plant Physiol.

J. Plant Physiol.

Liberation of amino acids in perennial ray grass during wilting

Biochem. J.

Expression of delta1-pyrroline-5-carboxylate synthetase gene during drought in rice (Oryza sativa L.)

Ind. J. Biochem. Biophys.

Correlation between the induction of a gene for delta 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress

Plant J.

Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris

Physiol. Plant.

Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis

Mol. Plant–Microbe Interact.

Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens

Proc. Natl. Acad. Sci. U. S. A.

Prokaryotic osmoregulation: genetics and physiology

Annu. Rev. Microbiol.

Metabolic implications of stress induced proline accumulation in plants

Plant Growth Regul.

Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance

Curr. Sci.

Proline accumulation in plants: a review

Amino Acids

Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis

Plant Physiol.

Eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant

Proc. Natl. Acad. Sci. U. S. A.

Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance

J. Exp. Bot.

Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance

J. Exp. Bot.

Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress

Plant Physiol.

Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis

Plant Mol. Biol.

Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis

Plant J.

A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyses the first two steps in proline biosynthesis in plants

Proc. Natl. Acad. Sci. U. S. A.

Subcellular location of delta-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean

Plant Physiol.

Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana

Plant Physiol.

Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis

Plant J

Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features

Physiol. Plant

A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis

Plant Cell

Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator

Review
Proline: a multifunctional amino acid