Amino Acids

, Volume 35, Issue 4, pp 753–759 | Cite as

Proline accumulation in plants: a review

Review Article

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.

Keywords

Osmotic stress Genetic engineering Proline toxicity P5CS P5CR P5CDH PDH 

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.

Notes

Acknowledgments

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

References

  1. 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 51:363–372PubMedCrossRefGoogle Scholar
  2. 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 129:169–180PubMedCrossRefGoogle Scholar
  3. 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 123:1279–1291PubMedCrossRefGoogle Scholar
  4. Chiang HH, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis thaliana (L) Heynh during development and in response to desiccation. Plant Cell Environ 18:1280–1290CrossRefGoogle Scholar
  5. 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 27:345–355PubMedCrossRefGoogle Scholar
  6. 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 16:3413–3425PubMedCrossRefGoogle Scholar
  7. 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 32:13–26CrossRefGoogle Scholar
  8. 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 138:123–132CrossRefGoogle Scholar
  9. Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67:780–784PubMedGoogle Scholar
  10. 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 17:343–350PubMedCrossRefGoogle Scholar
  11. 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 118:661–674PubMedCrossRefGoogle Scholar
  12. 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 38:755–764PubMedCrossRefGoogle Scholar
  13. Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102CrossRefGoogle Scholar
  14. Hellmann H, Funck D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol 122:357–367PubMedCrossRefGoogle Scholar
  15. 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 122:1129–1136PubMedCrossRefGoogle Scholar
  16. 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 89:9354–9358PubMedCrossRefGoogle Scholar
  17. 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 295:85–92PubMedCrossRefGoogle Scholar
  18. 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 114:1215–1224PubMedCrossRefGoogle Scholar
  19. 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 26:157–169PubMedCrossRefGoogle Scholar
  20. 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 108:1387–1394PubMedGoogle Scholar
  21. 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 8:1323–1335PubMedCrossRefGoogle Scholar
  22. 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 85:2036–2040PubMedCrossRefGoogle Scholar
  23. 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 94:1258–1264PubMedGoogle Scholar
  24. Lui J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596CrossRefGoogle Scholar
  25. 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 31:699–712PubMedCrossRefGoogle Scholar
  26. 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 128:73–83PubMedCrossRefGoogle Scholar
  27. 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 118:1233–1241PubMedCrossRefGoogle Scholar
  28. 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 18:185–193PubMedCrossRefGoogle Scholar
  29. 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 461:205–210PubMedCrossRefGoogle Scholar
  30. 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 44:541–548PubMedCrossRefGoogle Scholar
  31. 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 144:503–512PubMedCrossRefGoogle Scholar
  32. 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 253:334–341PubMedGoogle Scholar
  33. Phang JM (1985) The regulatory functions of proline and pyrroline-5-carboxylic acid. Curr Top Cell Regul 25:91–132PubMedGoogle Scholar
  34. Rayapati PJ, Stewart CR, Hack E (1989) Pyrroline-5-carboxylate reductase is in Pea (Pisum sativum L.) leaf chloroplasts. Plant Physiol 91:581–586PubMedCrossRefGoogle Scholar
  35. 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 8:1437–1446PubMedCrossRefGoogle Scholar
  36. 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 225:1313–1324PubMedCrossRefGoogle Scholar
  37. 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 104:19631–19636PubMedCrossRefGoogle Scholar
  38. 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 117:263–271PubMedCrossRefGoogle Scholar
  39. 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 209:1–5PubMedCrossRefGoogle Scholar
  40. 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 372:13–19PubMedCrossRefGoogle Scholar
  41. 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 254:104-109PubMedCrossRefGoogle Scholar
  42. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302PubMedCrossRefGoogle Scholar
  43. Siripornadulsil S, Train S, Verma DPS, Sayre RT (2002) Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14:2837–2847PubMedCrossRefGoogle Scholar
  44. Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060CrossRefGoogle Scholar
  45. 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 12:557–569PubMedCrossRefGoogle Scholar
  46. 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 53:11–28PubMedCrossRefGoogle Scholar
  47. 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 99:1642–1649PubMedGoogle Scholar
  48. Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103:771–781PubMedCrossRefGoogle Scholar
  49. 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 93:8787–8791PubMedCrossRefGoogle Scholar
  50. 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 57:201–212PubMedCrossRefGoogle Scholar
  51. Verslues PE, Kim YS, Zhu JK (2007) Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate:glyoxylate aminotransferase mutant. Plant Mol Biol 64:205–217PubMedCrossRefGoogle Scholar
  52. 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 25:3133–3143PubMedCrossRefGoogle Scholar
  53. 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 7:751–760PubMedCrossRefGoogle Scholar
  54. 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 38:1095–1102PubMedGoogle Scholar
  55. 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 270:20491–20496PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Laboratoire de Physiologie et de Génétique moléculaire des PlantesUniversité Libre de BruxellesBrusselsBelgium

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