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Multiple roles of proline in plant stress tolerance and development

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Abstract

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.

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References

  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:1022043000516

    Article  Google Scholar 

  2. Adams E, Frank L (1980) Metabolism of proline and the hydroxyprolines. Annu Rev Biochem 49: 1005–1061

    Article  CAS  Google Scholar 

  3. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55: 373–399

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  5. Atkinson DE (1977) Cellular Energy Metabolismand its regulation. NewYork, Academic Press

    Google Scholar 

  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.010940

    Article  CAS  Google Scholar 

  7. Baich A (1969) Proline synthesis in Escherichia coli. A proline-inhibitable glutamic acid kinase. Biochim Biophys Acta 192: 462–467

    CAS  Google Scholar 

  8. Bhaskaran S, Smith RH, Newton RJ (1985) Physiological changes in cultured sorghum cells in response to induced water stress. Plant Physiol 79: 266–269

    Article  CAS  Google Scholar 

  9. Bathurst NO (1954) The Amino-Acids of Grass Pollen. J Exp Bot 5: 253–256. DOI: 10.1093/jxb/5.2.253

    Article  CAS  Google Scholar 

  10. Beck T, Hall MN (1999) The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factrors. Nature 402: 689–692. DOI: 10.1038/45287

    Article  CAS  Google Scholar 

  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, USA

    Google Scholar 

  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/s00122-003-1322-0

    Article  CAS  Google Scholar 

  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/BJ20021266

    Article  CAS  Google Scholar 

  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: 1051–1053

    CAS  Google Scholar 

  15. Boggess SF, Paleg LG, Aspinall D (1975) Pyrroline 5-carboxylic acid dehydrogenase in barley, a proline-accumulating species. Plant Physiol 56: 259–262

    Article  CAS  Google Scholar 

  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.2005.11.035

    Article  CAS  Google Scholar 

  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: 287–292

    CAS  Google Scholar 

  18. Brown LM, Hellebust JA (1978) Sorbitol and proline as intracellular osmotic solutes in the green alga Stichococcus bacillaris. Can J Bot 56: 676–679

    Article  CAS  Google Scholar 

  19. Burton RS (1991) Regulation of proline synthesis in osmotic response: effects of protein synthesis inhibitors. J Exp Zool 259: 272–277

    Article  CAS  Google Scholar 

  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: 176–179

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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: 350–357

    Article  CAS  Google Scholar 

  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.2006.09.028

    Article  CAS  Google Scholar 

  24. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53: 121–147

    CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  26. Dann SG, Thomas G (2006) The amino acid sensitive Torpathway fromyeast tomammals. FEBS lett 580: 2821–2829. DOI: 10.1016/j.febslet.2006.04.068

    Article  CAS  Google Scholar 

  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: 299–305

    Article  CAS  Google Scholar 

  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.x

    Article  Google Scholar 

  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: 18673–18678

    Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  31. Duranton H, Wurtz R (1965) Conversion de l’ornithine en proline dans les tissues de topinanboan. Physiol Veg 3: 7–22

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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.2004.17.4.343

    Article  CAS  Google Scholar 

  34. Fafournoux P, Bruhat A, Jousse C (2000) Amino acid regulation of gene expression. Biochem J 351: 1–12

    Article  CAS  Google Scholar 

  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: 94–97

    CAS  Google Scholar 

  36. Forlani G, Scainelli D, Nielsen E (1997) Δ1-Pyrroline-5-Carboxylate Dehydrogenase from Cultured Cells of Potato (Purification and Properties) Plant Physiol 113 1413–1418

    CAS  Google Scholar 

  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: 661–674

    CAS  Google Scholar 

  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:1006015212391

    Article  CAS  Google Scholar 

  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: 10.1038/7777

    Article  CAS  Google Scholar 

  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: 938–945

    Article  CAS  Google Scholar 

  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: 489–493

    Google Scholar 

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

    Article  CAS  Google Scholar 

  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: 413–434

    Article  CAS  Google Scholar 

  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: 2979–2983

    Article  CAS  Google Scholar 

  45. Hellmann H, Funk D, Rentsch D, Frommer WB (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant towards exogenous proline application. Plant Physiol 123: 779–790

    Article  CAS  Google Scholar 

  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: 1129–1136

    Article  CAS  Google Scholar 

  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: 9354–9358

    Article  CAS  Google Scholar 

  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:1005702408601

    Article  CAS  Google Scholar 

  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: 1203–1207

    Article  CAS  Google Scholar 

  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: 73–79

    Article  CAS  Google Scholar 

  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: 161–169

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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: 1387–1394

    Google Scholar 

  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: 424–438

    Google Scholar 

  56. Kemble AR, MacPherson HT (1954) Liberation of amino acids in perennial rye grass during wilting. Biochem J 58: 46–59

    CAS  Google Scholar 

  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: 1323–1335

    Article  CAS  Google Scholar 

  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: 831–837

    Article  Google Scholar 

  59. Knight H, Trewavas AJ, Knight MR (1997) Calcium signalling in Arabidopsis responding to drought and salinity. Plant J 12: 1067–1078

    Article  CAS  Google Scholar 

  60. Krishna RV, Leisinger T (1979) Biosynthesis of proline in Pseudomonas aeruginosa. Partial purification and characterization of gamma-glutamyl kinase. Biochem J 181: 215–222

    CAS  Google Scholar 

  61. Krueger R, Jager H-J, Hintz Pahlich E (1986) Purification to homogeneity of pyrroline-5-carboxylate reductase of barley. Plant Physiol 80: 142–144

    Article  CAS  Google Scholar 

  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: 245–250

    Article  CAS  Google Scholar 

  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. Liu 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  CAS  Google Scholar 

  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, Berlin

    Google Scholar 

  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.105.035931

    Article  CAS  Google Scholar 

  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: 699–712

    Article  CAS  Google Scholar 

  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: 73–83

    Article  CAS  Google Scholar 

  69. Mansour M (1998) Protection of plasma membrane of onion epidermal cells by glycine betaine and proline against NaCl stress. Plant Physiol Biochem 36: 767–772

    Article  CAS  Google Scholar 

  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/s11103-007-9269-1

    Article  CAS  Google Scholar 

  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.1996.0338

    Article  CAS  Google Scholar 

  72. Majewska-Sawka A, Nothnagel EA (2000) Themultiple roles of arabinogalactanproteins in plant development. Plant Physiol 122: 3–9

    Article  CAS  Google Scholar 

  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.230445997

    Article  CAS  Google Scholar 

  74. Mestichelli LJJ, Gupta RN, Spencer ID (1979) The biosynthetic route from ornithine to proline. J Biol Chem 254: 640–647

    CAS  Google Scholar 

  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, USA

    Google Scholar 

  76. Moftah AE, Michel BE (1987) The effect of sodium chloride on solute potential and proline accumulation in soybean leaves. Plant Physiol 83: 238–240

    Article  CAS  Google Scholar 

  77. Moreno F, Ahuatzi D, Riera A, Palomino CA, Herrero P (2005) Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 33: 265–268

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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: 582–590

    Article  Google Scholar 

  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: 1497–1500

    Article  CAS  Google Scholar 

  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: 1233–1241

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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)01451-9

    Article  CAS  Google Scholar 

  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: 541–548

    Article  CAS  Google Scholar 

  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.106.095281

    Article  CAS  Google Scholar 

  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: 334–341

    CAS  Google Scholar 

  87. Poulin R, Larochelle J, Hellebust JA (1987) The regulation of amino acid metabolism during hyperosmotic stress in Acanthamoetla castellanii. J Exp Zool 243: 365–378

    Article  CAS  Google Scholar 

  88. Rayapati PJ, Stewart CR (1991) Solubilization of a proline dehydrogenase from maize (Zea mays L. mitochondria. Plant Physiol 95: 787–791

    Article  CAS  Google Scholar 

  89. Rhodes D, Handa S, Bressan RA (1986) Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol 82: 890–903

    Article  CAS  Google Scholar 

  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: 263–271

    Article  CAS  Google Scholar 

  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.288.5471.1613

    Article  CAS  Google Scholar 

  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)00935-3

    Article  Google Scholar 

  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/s004380050397

    Article  Google Scholar 

  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: 451–461

    CAS  Google Scholar 

  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: 377–391

    Article  CAS  Google Scholar 

  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: 6896–6901

    Article  CAS  Google Scholar 

  97. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125: 27–58

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  99. Snowalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–23

    Article  Google Scholar 

  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: 10.1186/1471-2229-8-32

    Article  CAS  Google Scholar 

  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 Sydney

    Google Scholar 

  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: 703–707

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  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: 1642–1649

    Article  CAS  Google Scholar 

  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.2005.06.002

    Article  CAS  Google Scholar 

  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.M308456200

    CAS  Google Scholar 

  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: 173–181

    Article  CAS  Google Scholar 

  109. Trovato M, Mauro ML, Costantino P, Altamura MM (1997) The rolD gene fromAgrobacterium rhizogenes is developmentally regulated in transgenic tobacco. Protoplasma 197: 111–120

    Article  CAS  Google Scholar 

  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.231320398

    Article  CAS  Google Scholar 

  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: 95–105

    Google Scholar 

  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: 102–109

    Google Scholar 

  113. Verbruggen N, Villarroel R, Van Montagu M (1993) Osmoregulation of a Pyrroline-5-Carboxylate Reductase Gene in Arabidopsis. Plant Physiol 103: 771–781

    Article  CAS  Google Scholar 

  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: 8787–8791

    Article  CAS  Google Scholar 

  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: 1349–1360

    Article  CAS  Google Scholar 

  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: 1125–1130

    Article  CAS  Google Scholar 

  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: 1256–1259

    Article  CAS  Google Scholar 

  118. Wang X (2005) Regulatory Functions of Phospholipase D and Phosphatidic Acid in Plant Growth, Development, and Stress Responses. Plant Physiol 139: 566–573

    Article  CAS  Google Scholar 

  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: 33–44

    CAS  Google Scholar 

  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.x

    Article  CAS  Google Scholar 

  121. Zhang HQ, Croes A, Linskens H (1982) Protein synthesis in germinating pollen of Petunia: Role of proline. Planta 154: 199–203

    Article  CAS  Google Scholar 

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  1. Dipartimento di Genetica e Biologia Molecolare, Università di Roma “La Sapienza”, P.le Aldo Moro 5, 00185, Roma, Italy

    Maurizio Trovato, Roberto Mattioli & Paolo Costantino

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  1. Maurizio Trovato
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  2. Roberto Mattioli
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  3. Paolo Costantino
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Correspondence to Maurizio Trovato.

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Trovato, M., Mattioli, R. & Costantino, P. Multiple roles of proline in plant stress tolerance and development. Rend. Fis. Acc. Lincei 19, 325–346 (2008). https://doi.org/10.1007/s12210-008-0022-8

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