Skip to main content

Advertisement

Log in

Proline accumulation in plants: a review

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Proline (Pro) accumulation is a common physiological response in many plants in response to a wide range of biotic and abiotic stresses. Controversy has surrounded the possible role(s) of proline accumulation. In this review, knowledge on the regulation of Pro metabolism during development and stress, results of genetic manipulation of Pro metabolism and current debate on Pro toxicity in plants are presented.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

ABA:

Abscissic acid

ABRE:

ABA responsive element

AS:

Antisense

At:

Arabidopsis thaliana

GFP:

Green fluorescent protein

GSA:

Glutamate semialdehyde

Nat-siRNAs:

Natural silencing RNA

PPP:

Pentose phosphate pathway

Pro:

Proline

PDH:

Pro dehydrogenase

P5C:

Pyrroline-5-carboxylate

P5CDH:

P5C dehydrogenase

P5CR:

P5C reductase

P5CS:

P5C synthase

RNAi:

RNA interference

ROS:

Reactive oxygen species

UTR:

Untranslated region.

References

  • Abraham E, Rigo G, Szekely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt stress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51:363–372

    Article  PubMed  CAS  Google Scholar 

  • Ayliffe MA, Roberts JK, Mitchell HJ, Zhang R, Lawrence GJ, Ellis JG, Pryor JT (2002) A plant gene up-regulated at rust infection sites. Plant Physiol 129:169–180

    Article  PubMed  CAS  Google Scholar 

  • Borsani O, Zhu J, Verslues PE, Sunkar R, Zhu JK (2005) Endogenous siRNAs derived from a pair of natural cisantisense transcripts regulate salt tolerance in Arabidopsis. Cell 123:1279–1291

    Article  PubMed  CAS  Google Scholar 

  • Chiang HH, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis thaliana (L) Heynh during development and in response to desiccation. Plant Cell Environ 18:1280–1290

    Article  CAS  Google Scholar 

  • Deuschle K, Funck D, Hellmann H, Daschner K, Binder S, Frommer WB (2001) A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potentiel role in protection from proline toxicity. Plant J 27:345–355

    Article  PubMed  CAS  Google Scholar 

  • Deuschle K, Funck D, Forlani G, Stransky H, Biehl A, Leister D, van der Graaff E, Kunze R, Frommer WB (2004) The role of Δ1 -pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16:3413–3425

    Article  PubMed  CAS  Google Scholar 

  • de Ronde JA, Spreeth MH, Cress WA (2000) Effect of antisense l-Δ1-pyrroline-5-carboxylate reductase transgenic soybean plants subjected to osmotic and drought stress. Plant Growth Regul 32:13–26

    Article  Google Scholar 

  • de Ronde JA, Laurie RN, Caetano T, Gray Ling MM, Kerepesi I (2004) Comparative study between transgenic and non-transgenic soybean lines proved transgenic lines to be more drought tolerant. Euphytica 138:123–132

    Article  Google Scholar 

  • Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67:780–784

    PubMed  CAS  Google Scholar 

  • Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced plant-pathogen incompatible interactions in Arabidospis. Mol Plant Microbe Interact 17:343–350

    Article  PubMed  CAS  Google Scholar 

  • Fujita T, Maggio A, Garcia-Rios M, Bressan RA, Csonka LN (1998) Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Δ1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiol 118:661–674

    Article  PubMed  CAS  Google Scholar 

  • Ginzberg I, Stein H, Kapulnik Y, Szabados L, Strizhov N, Schell J, Koncz C, Zilberstein A (1998) Isolation and characterization of two different cDNAs of Δ1-pyrroline-5-carboxylate synthase in alfalfa, transcriptionally induced upon salt stress. Plant Mol Biol 38:755–764

    Article  PubMed  CAS  Google Scholar 

  • Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 122:357–367

    Article  PubMed  CAS  Google Scholar 

  • Hong Z, Lakkineni K, Zhang Z, Verma DPS (2000) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    Article  PubMed  CAS  Google Scholar 

  • Hu CA, Delauney AJ, Verma DPS (1992) A bifunctional Δ1-enzyme-pyrroline-5-carboxylate synthetase catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358

    Article  PubMed  CAS  Google Scholar 

  • Hu CA, Donald SP, Yu J, Liu Z, Steel G, Obie C, Valle D, Phang JM (2007) Overexpression of proline oxidase induces proline-dependent and mitochondria-mediated apoptosis. Mol Cell Biochem 295:85–92

    Article  PubMed  CAS  Google Scholar 

  • Hua XJ, Van de Cotte B, Van Montagu M, Verbruggen N (1997) Developmental regulation of pyrroline-5-carboxylate reductase gene expression in Arabidopsis. Plant Physiol 114:1215–1224

    Article  PubMed  CAS  Google Scholar 

  • Hua XJ, Van de Cotte B, Van Montagu M, Verbruggen N (2001) The 5′ untranslated region of the At-P5R gene is involved in both transcriptional and post-transcriptional regulation. Plant J 26:157–169

    Article  PubMed  CAS  Google Scholar 

  • Kishor PBK, Hong Z, Miao CH, Hu CAA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase lncreases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    PubMed  CAS  Google Scholar 

  • Kiyosue T, Yoshiba Y, Yamaguchi-Shinozaki K, Shinozaki K. (1996) 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 8:1323–1335

    Article  PubMed  CAS  Google Scholar 

  • Kohl DH, Schubert KR, Carter MB, Hagedorn CH, Shearer G. (1988) Proline metabolism in N2-fixing root nodules: energy transfer and regulation of purine synthesis. Proc Natl Acad Sci USA 85:2036–2040

    Article  PubMed  CAS  Google Scholar 

  • Kohl DH, Lin JJ, Shearer G, Schubert KR (1990) Activities of the pentose phosphate pathway and enzymes of proline metabolism in legume root nodules. Plant Physiol 94:1258–1264

    PubMed  CAS  Google Scholar 

  • Lui J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596

    Article  Google Scholar 

  • Maggio A, Miyazaki S, Veronese P, Fujita T, Ibeas JI, Damsz B, Narasimhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31:699–712

    Article  PubMed  CAS  Google Scholar 

  • Mani S, Van de Cotte B, Van Montagu M, Verbruggen N (2002) Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiol 128:73–83

    Article  PubMed  CAS  Google Scholar 

  • Nakashima K, Satoh R, Kiyosue T, Yamagashi-Shinozaki K, Shinozaki K (1998) A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. Plant Physiol 118:1233–1241

    Article  PubMed  CAS  Google Scholar 

  • Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tsukaya H, Kakubari Y, Yamagushi-Shinozaki K, Shinozaki K (1999a) Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J 18:185–193

    Article  PubMed  CAS  Google Scholar 

  • Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999b) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210

    Article  PubMed  CAS  Google Scholar 

  • Nanjo T, Fujita M, Seki M, Kato T, Tabata S, Shinozaki K (2003) Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell Physiol 44:541–548

    Article  PubMed  CAS  Google Scholar 

  • Parre E, Ghars MA, Leprince AS, Thiery L, Lefebvre D, Bordenave M, Richard L, Mazars C, Abdelly C, Savouré A (2007) Calcium signaling via phospholipase C is essential for proline accumulation upon ionic but not nonionic hyperosmotic stresses in Arabidopsis. Plant Physiol 144:503–512

    Article  PubMed  CAS  Google Scholar 

  • Peng Z, Lu Q, Verma DPS (1996) Reciprocal regulation of 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Gen Genet 253:334–341

    PubMed  CAS  Google Scholar 

  • Phang JM (1985) The regulatory functions of proline and pyrroline-5-carboxylic acid. Curr Top Cell Regul 25:91–132

    PubMed  CAS  Google Scholar 

  • Rayapati PJ, Stewart CR, Hack E (1989) Pyrroline-5-carboxylate reductase is in Pea (Pisum sativum L.) leaf chloroplasts. Plant Physiol 91:581–586

    Article  PubMed  CAS  Google Scholar 

  • Rentsch D, Hirner B, Schmelzer E, Frommer WB (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8:1437–1446

    Article  PubMed  CAS  Google Scholar 

  • Ribarits A, Abdullaev A, Tashpulatov A, Richter A,·Heberle-Bors E, Touraev A (2007) Two tobacco proline dehydrogenases are differentially regulated and play a role in early plant development. Planta 225:1313–1324

    Article  PubMed  CAS  Google Scholar 

  • Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636

    Article  PubMed  CAS  Google Scholar 

  • Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-δ-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiol 117:263–271

    Article  PubMed  CAS  Google Scholar 

  • Saradhi P, Alia P, Arora S, Prasad KV (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem Biophys Res Commun 209:1–5

    Article  PubMed  CAS  Google Scholar 

  • Savouré A, Jaoua S, Hua XJ, Ardiles W, Van Montagu M, Verbruggen N (1995) Isolation, characterization, and chromosomal location of a gene encoding the 1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett 372:13–19

    Article  PubMed  Google Scholar 

  • Savouré A, Hua XJ, Bertauche N, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of the proline biosynthesis upon cold and osmotic stresses in Arabidopsis thaliana. Mol Gen Genet 254:104-109

    Article  PubMed  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  PubMed  CAS  Google Scholar 

  • Siripornadulsil S, Train S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060

    Article  CAS  Google Scholar 

  • Strizhov N, Abraham E, Okresz L, Blickling S, Zilberstein A, Schell J, Koncz C, Szabados L (1997) 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 12:557–569

    Article  PubMed  CAS  Google Scholar 

  • Székely G, Abraham E, Cseplo A, Rigo G, Zsigmond L, Csiszar J, Ayaydin F, Strizhov N, Jasik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53:11–28

    Article  PubMed  CAS  Google Scholar 

  • Szoke A, Miao GH, Hong Z, Verma DPS (1992) Subcellular location of Δ1-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean. Plant Physiol 99:1642–1649

    PubMed  CAS  Google Scholar 

  • Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103:771–781

    Article  PubMed  CAS  Google Scholar 

  • Verbruggen N, Hua XJ, May M, Van Montagu M (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proc Natl Acad Sci USA 93:8787–8791

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Bray EA (2006) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Kim YS, Zhu JK (2007) Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate:glyoxylate aminotransferase mutant. Plant Mol Biol 64:205–217

    Article  PubMed  CAS  Google Scholar 

  • Weltmeier F, Ehlert A, Mayer CS, Dietrich K, Wang X, Schutze K, Alonso R, Harter K, Vicente-Carbajosa J, Droge-Laser W (2006) Combinatorial control of Arabidopsis proline dehydrogenase transcription by specific heterodimerisation of bZIP transcription factors. EMBO J 25:3133–3143

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, Mizoguchi T, Yamaguchi-Shinozaki K, Wada K, Harada Y, Shinozaki K (1995) Correlation between the induction of a gene for Δ1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J 7:751–760

    Article  PubMed  CAS  Google Scholar 

  • Yoshiba Y, Kiyosue T, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (1997) Regulation of levels of proline as an osmolyte in plants under water stress. Plant Cell Physiol 38:1095–1102

    PubMed  CAS  Google Scholar 

  • Zhang CS, Lu Q, Verma DPS (1995) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. J Biol Chem 270:20491–20496

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank the Belgian Science Policy for financial support (project PAIVI/33, return grant of C.H).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nathalie Verbruggen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verbruggen, N., Hermans, C. Proline accumulation in plants: a review. Amino Acids 35, 753–759 (2008). https://doi.org/10.1007/s00726-008-0061-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-008-0061-6

Keywords

Navigation