, Volume 19, Issue 4, pp 325–346 | Cite as

Multiple roles of proline in plant stress tolerance and development

  • Maurizio Trovato
  • Roberto Mattioli
  • Paolo Costantino


The recent progresses in the research on proline will be described, focusing on plants and covering proline metabolism and signal transduction as well as the role of this imino acid in stress response. Furthermore, the recently described developmental role of proline in flowering and reproduction will be illustrated and discussed.


Flowering development proline P5CS1 stress 

Subject codes



Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Ábrahám E, Rigó G, Székely G, Nagy R, Koncz C, Szabados L (2003) Light-dependent induction of proline biosynthesis by abscisic acid and salt sress is inhibited by brassinosteroid in Arabidopsis. Plant Mol Biol 51: 363–372 DOI: 10.1023/A:1022043000516CrossRefGoogle Scholar
  2. 2.
    Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49: 1005–1061CrossRefGoogle Scholar
  3. 3.
    Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55: 373–399CrossRefGoogle Scholar
  4. 4.
    Armengaud P, Thiery L, Buhot N, Grenier-De March G, Savouré A (2004) Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol Plantarum 120: 442–450. DOI: 10.1111/j.00319317.2004.00251.xCrossRefGoogle Scholar
  5. 5.
    Atkinson DE (1977) Cellular Energy Metabolismand its regulation. NewYork, Academic PressGoogle Scholar
  6. 6.
    Ayliffe MA, Roberts JK, Mitchell HJ, Zhang R, Lawrence GJ, Ellis JG, Pryor TJ (2002) A plant gene up-regulated at rust infection sites. Plant Physiol 129: 169–180. DOI: 10.1104/pp.010940CrossRefGoogle Scholar
  7. 7.
    Baich A (1969) Proline synthesis in Escherichia coli. A proline-inhibitable glutamic acid kinase. Biochim Biophys Acta 192: 462–467Google Scholar
  8. 8.
    Bhaskaran S, Smith RH, Newton RJ (1985) Physiological changes in cultured sorghum cells in response to induced water stress. Plant Physiol 79: 266–269CrossRefGoogle Scholar
  9. 9.
    Bathurst NO (1954) The Amino-Acids of Grass Pollen. J Exp Bot 5: 253–256. DOI: 10.1093/jxb/5.2.253CrossRefGoogle Scholar
  10. 10.
    Beck T, Hall MN (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factrors. Nature 402: 689–692. DOI: 10.1038/45287CrossRefGoogle Scholar
  11. 11.
    Bernier G, Kinet JM, Sachs RM (1981) The Physiology of Flowering, Vol. 2. Transition to reproductive growth. CRC Press, 157–159 Boca Raton, FL, USAGoogle Scholar
  12. 12.
    Bettini P, Michelotti S, Bindi D, Giannini R, Capuana M, Buiatti M (2003) Pleiotropic effect of the insertion of Agrobacterium rhizogenes rolD gene in tomato (Lycopersicon esculentum Mill). Theor Appl Genet 107: 831–836. DOI: 10.1007/s00122-003-1322-0CrossRefGoogle Scholar
  13. 13.
    Beugnet A, Tee AR, Taylor PM, Proud CG (2003) Regulation of targets of mTOR (mammalian target of rapamycin) signalling by intracellular amino acid availability. Biochem J 372: 555–566. DOI: 10.1042/BJ20021266CrossRefGoogle Scholar
  14. 14.
    Blum A, Munns R, Passioura JB, Turner NC, Sharp PE, Boyer JS, Nguyen HT, Hsiao TC, Verma DPS, Hong Z (1996) Genetically engineered plants resistant to soil drying and salt stress: How to interpret osmotic relations? Plant Physiol 110: 1051–1053Google Scholar
  15. 15.
    Boggess SF, Paleg LG, Aspinall D (1975) Pyrroline 5-carboxylic acid dehydrogenase in barley, a proline-accumulating species. Plant Physiol 56: 259–262CrossRefGoogle Scholar
  16. 16.
    Borsani O, Zhu J, Versules PE, Sunkar R, Zhu J-K (2005) Endogenous siRNA derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279–1291. DOI: 10.1016/j.cell.2005.11.035CrossRefGoogle Scholar
  17. 17.
    Briens M, Larher F (1982) Osmoregulation in halophytic higher plants: a comparative study of soluble carbohydrates, polyols, betaines and free proline. Plant Cell Environ 5: 287–292Google Scholar
  18. 18.
    Brown LM, Hellebust JA (1978) Sorbitol and proline as intracellular osmotic solutes in the green alga Stichococcus bacillaris. Can J Bot 56: 676–679CrossRefGoogle Scholar
  19. 19.
    Burton RS (1991) Regulation of proline synthesis in osmotic response: effects of protein synthesis inhibitors. J Exp Zool 259: 272–277CrossRefGoogle Scholar
  20. 20.
    Chandler SF, Thorpe PA (1987) Proline accumulation and sodium sulfate tolerance in callulus culture of Brassica napus L. cv Westar. Plant Cell Rep 6: 176–179CrossRefGoogle Scholar
  21. 21.
    Chiang HH, Dandekar AM (1995) Regulation of proline accumulation in Arabidopsis during development and in response to dessication. Plant Cell Environ 18: 1280–1290. DOI: 10.1111/j.1365-3040.1995.tb00187.xCrossRefGoogle Scholar
  22. 22.
    Chilson OP, Kelly-Chilson AE, Siegel NR (1991) Pyrroline-5-carboxylate reductase in soybean nodules: isolation/partial primary structure/evidence for isozymes. Arch Biochem Biophys 288: 350–357CrossRefGoogle Scholar
  23. 23.
    Cho YH, Yoo SD, Sheen J (2006) Regulatory functions of nuclear hexokinase1 complex in glucose signaling. Cell 127: 579–589. DOI: 10.1016/j.cell.2006.09.028CrossRefGoogle Scholar
  24. 24.
    Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53: 121–147Google Scholar
  25. 25.
    Chung JS, Zhu JK, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J. 53: 554–565. DOI: 10.1111/j.1365-313X.2007.03364.xCrossRefGoogle Scholar
  26. 26.
    Dann SG, Thomas G (2006) The amino acid sensitive Torpathway fromyeast tomammals. FEBS lett 580: 2821–2829. DOI: 10.1016/j.febslet.2006.04.068CrossRefGoogle Scholar
  27. 27.
    Delauney AJ, Verma DPS (1990) A soybean gene encoding Δ1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol. Gen. Genet 221: 299–305CrossRefGoogle Scholar
  28. 28.
    Delanauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4: 215–223. DOI: 10.1046/j.1365-313X.1993.04020215.xCrossRefGoogle Scholar
  29. 29.
    Delanauney AJ, Hu CAA, Kavi Kishor PV, Verma DPS (1993) Cloning of ornithine δ-aminotransferase cDNAfrom Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of Proline Biosynthesis. J Biol Chem 268: 18673–18678Google Scholar
  30. 30.
    Deuschle K, Funck D, Hellmann H, Däschner K, Binder S, Frommer WB (2001) A nuclear gene encodingmitochondrial Δ1-pyrroline-5-carboxylate dehydrogenase and its potential role in protection fromproline toxicity. Plant J 27: 345–56. DOI: 10.1046/j.1365-313X.2001.01101.xCrossRefGoogle Scholar
  31. 31.
    Duranton H, Wurtz R (1965) Conversion de l’ornithine en proline dans les tissues de topinanboan. Physiol Veg 3: 7–22Google Scholar
  32. 32.
    Elthon TE, Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67: 780–784CrossRefGoogle Scholar
  33. 33.
    Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez ME (2004) Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant Microbe Interact 17: 343–350. DOI: 10.1094/MPMI.2004.17.4.343CrossRefGoogle Scholar
  34. 34.
    Fafournoux P, Bruhat A, Jousse C (2000) Amino acid regulation of gene expression. Biochem J 351: 1–12CrossRefGoogle Scholar
  35. 35.
    Floyd RA Nagy ZS (1984) Formation of long-lived hydroxyl free radical adducts of proline and hydroxyproline in a Fenton reaction. Biochem Biophys Acta 790: 94–97Google Scholar
  36. 36.
    Forlani G, Scainelli D, Nielsen E (1997) Δ1-Pyrroline-5-Carboxylate Dehydrogenase from Cultured Cells of Potato (Purification and Properties) Plant Physiol 113 1413–1418Google Scholar
  37. 37.
    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. Proc Natl Acad Sci USA 118: 661–674Google Scholar
  38. 38.
    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 delta1-pyrroline-5-carboxylate synthase in alfalfa, transcriptionally induced upon salt stress. PlantMol Biol 38: 755–764. DOI: 10.1023/A:1006015212391CrossRefGoogle Scholar
  39. 39.
    Gogos JA, Santha M, Takacs Z, Beck KD, Luine V, Lucas LR, Nadler JV, Karayiorgou M (1999) The gene encoding proline dehydrogenase modulates sensorimotor gating in mice. Nat Genet 21: 434–439. DOI: 10.1038/7777CrossRefGoogle Scholar
  40. 40.
    Handa S, Handa AK, Hasegawa PM, Bressan RA (1986) Proline accumulation and the adaptation of cultured plant cells to water stress. Plant Physiol 80: 938–945CrossRefGoogle Scholar
  41. 41.
    Hanson AD, Nelsen CE, Pedersen AR, Everson AH (1977) Capacity for proline accumulation duringwater stress in barley and its implication for breedings for drought resistance. Crop Sci 19: 489–493Google Scholar
  42. 42.
    Hare PD, Cress WA (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21: 79–102CrossRefGoogle Scholar
  43. 43.
    Hare PD, Cress WA Van Staden J (1999) Prolyne synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot 50: 413–434CrossRefGoogle Scholar
  44. 44.
    Hayward DC, Delaney SJ, Campbell HD, Ghysen A, Benzer S, Kasprzak AB, Cotsell JN, Young IG, Gabor-Miklos GL (1993) The sluggish — A gene of Drosophila melanogaster is expressed in the nervous system and encodes proline oxidase, a mitochondrial enzyme involved in glutamate biosynthesis. Proc Natl Acad Sci USA 90: 2979–2983CrossRefGoogle Scholar
  45. 45.
    Hellmann H, Funk D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant towards exogenous proline application. Plant Physiol 123: 779–790CrossRefGoogle Scholar
  46. 46.
    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: 1129–1136CrossRefGoogle Scholar
  47. 47.
    Hu CAA, Delauney AJ, Verma DPS (1992) A bifunctional enzyme Δ1-pyrroline-5-carboxylate synthetase catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89: 9354–9358CrossRefGoogle Scholar
  48. 48.
    Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K (1997) Characterization of the gene for Δ1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Molecular Biology 33: 857–865. DOI: 10.1023/A:1005702408601CrossRefGoogle Scholar
  49. 49.
    Inana G, Totsuka S, Redmond M, Dougherty T, Nagle J, Shiono T, Ohura T, Koninami E, Katunuma N (1986) Molecular cloning of human ornithine aminotransferase mRNA. Proc Natl Acad Sci USA 83: 1203–1207CrossRefGoogle Scholar
  50. 50.
    Kandpal RP, Rao NA (1985) Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine coracana) seedlings during water stress and the effect of proline on protein biosynthesis. Plant Sci 40: 73–79CrossRefGoogle Scholar
  51. 51.
    Kaneshiro ES, Holz GG Jr, Dunham PB (1969) Osmoregulation in a marine ciliate, Miamiensis avidus. II. Regulation of intracellular free amino acids. Biol Bull 137: 161–169CrossRefGoogle Scholar
  52. 52.
    Kant S, Kant P, Raveh E, Barak S (2006) Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila. Plant Cell Environ 29: 1220–1234. DOI: 10.1111/j.1365-3040.2006.01502.xCrossRefGoogle Scholar
  53. 53.
    Kant P, Gordon M, Kant S, Zolla G, Davydov O, Heimer YM, Chalifa-Caspi V, Shaked R, Barak S (2008) Functional-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses.Plant Cell Environ 31: 697–714. DOI: 10.1111/j.1365-3040.2008.01779.xCrossRefGoogle Scholar
  54. 54.
    Kavi Kishor PB, Hong Z, Miao G-H, Hu C-AA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108: 1387–1394Google Scholar
  55. 55.
    Kavi Kishor PB, Sangam S, Amrutha RN, Sri Laxmi P, Naidu KR, Rao KRSS, Rao S, Reddy P, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr Science 88: 424–438Google Scholar
  56. 56.
    Kemble AR, MacPherson HT (1954) Liberation of amino acids in perennial rye grass during wilting. Biochem J 58: 46–59Google Scholar
  57. 57.
    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: 1323–1335CrossRefGoogle Scholar
  58. 58.
    Kohl DH, Kennelly EJ, Zhu Y, Schubert KR, Shearer G (1991) Proline accumulation, nitrogenase (C2 H2 reducing) activity and activities of enzymes related to proline metabolism in drought-stressed soybean nodules. J Exp Bot 240: 831–837CrossRefGoogle Scholar
  59. 59.
    Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis responding to drought and salinity. Plant J 12: 1067–1078CrossRefGoogle Scholar
  60. 60.
    Krishna RV, Leisinger T (1979) Biosynthesis of proline in Pseudomonas aeruginosa. Partial purification and characterization of gamma-glutamyl kinase. Biochem J 181: 215–222Google Scholar
  61. 61.
    Krueger R, Jager H-J, Hintz Pahlich E (1986) Purification to homogeneity of pyrroline-5-carboxylate reductase of barley. Plant Physiol 80: 142–144CrossRefGoogle Scholar
  62. 62.
    LaRosa PC, Rhodes D, Rhodes JC, Bressan RA, Csonka LN (1991) Elevated Accumulation of Proline in NaCI-Adapted Tobacco Cells Is Not Due to Altered Δ1-Pyrroline-5-Carboxylate Reductase. Plant Physiol 96: 245–250CrossRefGoogle Scholar
  63. 63.
    Leisinger T (1987) Biosynthesis of proline in Escherichia coli and Salmonella typhimurium. In Neidhart FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Cellular andMolecular Biology. 345–351, American Society for Microbiology, Washington D.C.Google Scholar
  64. 64.
    Liu 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
  65. 65.
    Low PS (1985) Molecular basis of the biological compatibility of nature’s osmolytes. In Gilles R, Gilles-Baillien M (eds) Transport Processes, Iono- and Osmoregulation. 469–477, Springer-Verlag, BerlinGoogle Scholar
  66. 66.
    Mahfouz MM, Kim S, Delauney AJ, Verma DPS (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18: 477–490. DOI: 10.1105/tpc.105.035931CrossRefGoogle Scholar
  67. 67.
    Maggio A, Miyazaki S, Veronese P, Fuijita T, Ibeas JI, Damsz B, Narasmhan ML, Hasegawa PM, Joly RJ, Bressan RA (2002) Does proline accumulation play an active role in stress-induced growth reduction? Plant J 31: 699–712CrossRefGoogle Scholar
  68. 68.
    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: 73–83CrossRefGoogle Scholar
  69. 69.
    Mansour M (1998) Protection of plasma membrane of onion epidermal cells by glycine betaine and proline against NaCl stress. Plant Physiol Biochem 36: 767–772CrossRefGoogle Scholar
  70. 70.
    Mattioli R, Marchese D, D’Angeli S, Altamura MM, Costantino P, Trovato M (2008) Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol Biol 66: 277–288. DOI: 10.1007/s11103-007-9269-1CrossRefGoogle Scholar
  71. 71.
    Mauro ML, Trovato M, De Paolis A, Gallelli A, Costantino P, Altamura MM (1996) The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Dev Biol 180: 693–700. DOI: 10.1006/dbio.1996.0338CrossRefGoogle Scholar
  72. 72.
    Majewska-Sawka A, Nothnagel EA (2000) Themultiple roles of arabinogalactanproteins in plant development. Plant Physiol 122: 3–9CrossRefGoogle Scholar
  73. 73.
    Maxwell SA, Davis GE (2000) Differential gene expression in p53-mediated apoptosis-resistant vs. apoptosis-sensitive tumor cell lines. Proc Natl Acad Sci USA 97: 13009–13014. DOI: 10.1073/pnas.230445997CrossRefGoogle Scholar
  74. 74.
    Mestichelli LJJ, Gupta RN, Spencer ID (1979) The biosynthetic route from ornithine to proline. J Biol Chem 254: 640–647Google Scholar
  75. 75.
    Meyer AD, Tempé J, Costantino P (2000) Hairy Root: AMolecularOverview. Functional Analysis of Agrobacterium rhizogenes T-DNA Genes. In Stacey G and Keen NT (eds.), Plant-Microbe Interactions, APS Press, 5: 93–139, Minneapolis, MA, USAGoogle Scholar
  76. 76.
    Moftah AE, Michel BE (1987) The effect of sodium chloride on solute potential and proline accumulation in soybean leaves. Plant Physiol 83: 238–240CrossRefGoogle Scholar
  77. 77.
    Moreno F, Ahuatzi D, Riera A, Palomino CA, Herrero P (2005) Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 33: 265–268CrossRefGoogle Scholar
  78. 78.
    Munnik T, Meijer HJ, Ter Riet B, Hirt H, Frank W, Bartels D, Musgrave A (2000) Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J 22: 147–154. DOI: 10.1046/j.1365-313x.2000.00725.xCrossRefGoogle Scholar
  79. 79.
    Munoz FJ, Dopico B, Labrador E (1988) A cDNA encoding a proline-rich protein from Cicer arietinum. Changes in expression during development and abiotic stress. Physiol Plant 102: 582–590CrossRefGoogle Scholar
  80. 80.
    Mutters RG, Ferreira LGR, Hall AE (1989) Proline content of the anthers and pollen of heat-tolerant and heat-sensitive cowpea subjected to different temperatures. Crop Sci 29: 1497–1500CrossRefGoogle Scholar
  81. 81.
    Nakashima K, Satoh R, Kiyosue T, Yamaguchi-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: 1233–1241CrossRefGoogle Scholar
  82. 82.
    Nanjo T, Kobayashi M, Yoshiba Y, Sanada Y, Wada K, Tukaya H, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999a) Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis. Plant J 18: 185–193. DOI: 10.1046/j.1365-313X.1999.00438.xCrossRefGoogle Scholar
  83. 83.
    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. FEBS Lett 461: 205–210. DOI: 10.1016/S0014-5793(99)01451-9CrossRefGoogle Scholar
  84. 84.
    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: 541–548CrossRefGoogle Scholar
  85. 85.
    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. J Plant Physiol 144: 503–512. DOI: 10.1104/pp.106.095281CrossRefGoogle Scholar
  86. 86.
    Peng Z, Lu Q, Verma DP (1996) Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Mol Gen Genet 253: 334–341Google Scholar
  87. 87.
    Poulin R, Larochelle J, Hellebust JA (1987) The regulation of amino acid metabolism during hyperosmotic stress in Acanthamoetla castellanii. J Exp Zool 243: 365–378CrossRefGoogle Scholar
  88. 88.
    Rayapati PJ, Stewart CR (1991) Solubilization of a proline dehydrogenase from maize (Zea mays L. mitochondria. Plant Physiol 95: 787–791CrossRefGoogle Scholar
  89. 89.
    Rhodes D, Handa S, Bressan RA (1986) Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol 82: 890–903CrossRefGoogle Scholar
  90. 90.
    Roosens NH, Thu TT, Iskandar HM, Jacobs M (1998) Isolation of the ornithine-delta-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis. Plant Physiol 117: 263–271CrossRefGoogle Scholar
  91. 91.
    Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer S, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target Genes in reproductive development of Arabidopsis. Science 288: 1613–1616. DOI: 10.1126/science.288.5471.1613CrossRefGoogle Scholar
  92. 92.
    Savouré A, Jaoua S, Hua XJ, Ardiles W, Van Montagu M, Verbruggen N (1995) Isolation and characterization, and chromosomal location of a gene encoding the Δ1-pyrroline-5-carboxylate synthetase in Arabidopsis. FEBS Lett 372: 13–19. DOI: 10.1016/0014-5793(95)00935-3CrossRefGoogle Scholar
  93. 93.
    Savouré A, Hua XJ, Bertauche N, Van Montagu M, Verbruggen N (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stress. Molecular and General Genetics 254: 104–109. DOI: 10.1007/s004380050397CrossRefGoogle Scholar
  94. 94.
    Schobert B (1977) The influence of water stress on the metabolism of diatoms. II. Proline accumulation under different conditions of stress and light. Z Pflanzenphysiol 85: 451–461Google Scholar
  95. 95.
    Schwacke R, Grallath S, Breitkreuz KE, Stransky H, Frommer WB, Rentsch D (1999) LeProT1, a transporter for proline, glycine betaine, and γ-amino butyric acid in tomato pollen. Plant Cell 11: 377–391CrossRefGoogle Scholar
  96. 96.
    Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A. 97: 6896–6901CrossRefGoogle Scholar
  97. 97.
    Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125: 27–58CrossRefGoogle Scholar
  98. 98.
    Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry. 28: 1057–1060CrossRefGoogle Scholar
  99. 99.
    Snowalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23CrossRefGoogle Scholar
  100. 100.
    Spollen WG, Tao W, Valliyodan B, Chen K, Hejlek LG, Kim JJ, LeNoble ME, Zhu J, Bohnert HJ, Henderson D, Schachtman DP, Davis GE, Springer GK, Sharp RE, Nguyen HT (2008) Spatial distribution of transcript changes in the maize primary root elongation zone at low water potential. BMC Plant Biol 8: 1–32. DOI: 10.1186/1471-2229-8-32CrossRefGoogle Scholar
  101. 101.
    Stewart CR (1981) Proline accumulation: biochemical aspects. In Paleg LG and Aspinall D (eds) Physiology and Biochemistry of Drought Resistance in Plants, Academic Press 243–259 SydneyGoogle Scholar
  102. 102.
    Stewart CR, Voetberg G, Rapayati PJ (1986) The effects of benzyladenine, and cordycepin on wilting-induced abscisic acid and proline accumulation and abscisic acid- and salt induced proline accumulation in barley leaves. Plant Physiolo 82: 703–707CrossRefGoogle Scholar
  103. 103.
    Strizhov N, Ábrahám E, Ökresz 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. DOI: 10.1046/j.1365-313X.1997.00557.xCrossRefGoogle Scholar
  104. 104.
    Székely G, Ábrahám E, Cséplo Á, Rigo G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik 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. DOI: 10.1111/j.1365-313X.2007.03318.xCrossRefGoogle Scholar
  105. 105.
    Szoke A, Miao G-H, Hong Z, Verma DPS (1992). Subcellular localization of Δ1-pyrroline-5-carboxylate reductase in root/lnodule and leaf of soybean. Plant Physiol 99: 1642–1649CrossRefGoogle Scholar
  106. 106.
    Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10: 368–375. DOI: 10.1016/j.tplants.2005.06.002CrossRefGoogle Scholar
  107. 107.
    Thiery L, Leprince A-S, Lefebvre D, Ghars MA, Debarbieux E, Savouré A (2004) Phospholipase D is a negative regulator of proline biosynthesis in Arabidopsis. J Biochem Chem 279: 14812–14818. DOI: 10.1074/jbc.M308456200Google Scholar
  108. 108.
    Treichel S (1986) The influence of NaCl on delta1-pyrroline-5-carboxylate reductase in proline-accumulating cell suspension cultures of Mesembryanthemum nodiflorum and other halophytes. Plant Physiol 67: 173–181CrossRefGoogle Scholar
  109. 109.
    Trovato M, Mauro ML, Costantino P, Altamura MM (1997) The rolD gene fromAgrobacterium rhizogenes is developmentally regulated in transgenic tobacco. Protoplasma 197: 111–120CrossRefGoogle Scholar
  110. 110.
    Trovato M, Maras B, Linhares F, Costantino P (2001) The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proc Natl Acad Sci USA 98: 13449–13453. DOI: 10.1073/pnas.231320398CrossRefGoogle Scholar
  111. 111.
    Vansuyt G, Vallee J-C, Prevost J (1979) La pyrroline-5-carboxylate réductase et la proline déhydrogénase chez Nicotiana tabacum var. Xanthi n.c. en fonction de son développement. Physiol Veg 19: 95–105Google Scholar
  112. 112.
    Venekamp JH, Koot JTM (1988) The sources of free proline and asparagine in field bean plants, Vicia faba L., during and after a short period of water withholding. J Plant Physiol 32: 102–109Google Scholar
  113. 113.
    Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a Pyrroline-5-Carboxylate Reductase Gene in Arabidopsis. Plant Physiol 103: 771–781CrossRefGoogle Scholar
  114. 114.
    Verbruggen N, Hua X-J, 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: 8787–8791CrossRefGoogle Scholar
  115. 115.
    Verslues PE, Sharp RE (1999) Proline Accumulation in Maize (Zea mays L.) Primary Roots at Low Water Potentials. II. Metabolic Source of Increased Proline Deposition in the Elongation Zone. Plant Physiology 119: 1349–1360CrossRefGoogle Scholar
  116. 116.
    Voetberg GS, Sharp RE (1991) Growth of the maize primary root tip at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol 96: 1125–1130CrossRefGoogle Scholar
  117. 117.
    Walton EF, Clark CJ, Boldingh HL (1991) Effect of hydrogen cyanamide on amino acid profiles in kiwifruit buds during bud-break. Plant Physiol 97: 1256–1259CrossRefGoogle Scholar
  118. 118.
    Wang X (2005) Regulatory Functions of Phospholipase D and Phosphatidic Acid in Plant Growth, Development, and Stress Responses. Plant Physiol 139: 566–573CrossRefGoogle Scholar
  119. 119.
    White FF, Taylor BH, Huffmman GA, Gordon MP, Nester EW (1985) Molecular and genetic analysis of the transferred DNA regions of the root inducing plasmid of Agrobacterium rhizogenes. J Bacteriol 164: 33–44Google Scholar
  120. 120.
    Yoshiba Y, Kiyosue T, Katagiri T, Ueda H, 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 under osmotic stress. Plant J 7: 751–760. DOI: 10.1046/j.1365-313X.1995.07050751.xCrossRefGoogle Scholar
  121. 121.
    Zhang HQ, Croes A, Linskens H (1982) Protein synthesis in germinating pollen of Petunia: Role of proline. Planta 154: 199–203CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Italia 2008

Authors and Affiliations

  • Maurizio Trovato
    • 1
  • Roberto Mattioli
    • 1
  • Paolo Costantino
    • 1
  1. 1.Dipartimento di Genetica e Biologia MolecolareUniversità di Roma “La Sapienza”RomaItaly

Personalised recommendations