Metabolic implications of stress-induced proline accumulation in plants

Plant Growth Regulation

Volumn 21, Issue 2, 1997, Pages 79-102

  Hare, P D ^a   Cress, W A ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

environmental stress; metabolic regulation; oxidative pentose phosphate pathway; proline; pyrroline 5 carboxylate reductase; signal transduction

Indexed keywords

EID: 0030904878     PISSN: 01676903     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1005703923347     Document Type: Article

References (179)

1. Alia and Pardha Saradhi P (1991) Proline accumulation under heavy metal stress. J Plant Physiol 138: 554-558
2. Alia and Pardha Saradhi P (1993) Suppression in mitochondrial electron transport is the prime cause behind stress induced proline accumulation. Biochem Biophys Res Commun 193: 54-58
3. Alia, Pardha Saradhi P and Mohanty P (1991) Proline enhances primary photochemical activities in isolated thylakoid membranes of Brassica juncea by arresting photo- inhibitory damage. Biochem Biophys Res Commun 181: 1238-1244
4. Aloni B and Rosenshtein G (1982) Effect of flooding on tomato cultivars: The relationship between proline accumulation and other morphological and physiological changes. Physiol Plant 56: 513-517
5. Anbazhagan M, Krishnamurthy R and Bhagwat KA (1988) Proline: An enigmatic indicator of air pollution tolerance in rice cultivars. J Plant Physiol 133: 122-123
6. Ap Rees T (1990) Carbon metabolism in mitochondria. In: Dennis DT and Turpin DH (eds) Plant Physiology: Biochemistry and Molecular Biology, p 116. London: Longman
7. Arakawa T and Timasheff SN (1983) Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arch Biochem Biophys 244: 169-177
8. Arakawa T and Timasheff SN (1985) The stabilisation of proteins by osmolytes. Biophys J 47: 411-414
9. Argandona V and Pahlich E (1991) Water stress on proline content and enzyme activities in barley seedlings. Phytochemistry 30: 1093-1094
10. Aro E-M, McCaffery S and Anderson JM (1993a) Photoinhibition and D1 degradation in peas acclimated to different growth irradiances. Plant Physiol 103: 835-843
11. Aro E-M, Virgin I and Andersson B (1993b) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
12. Atkinson DE (1977) Cellular Energy Metabolism and Its Regulation. New York: Academic Press
13. Auderset G, Gahan PB ,Dawson AL and Greppin H (1980) Glucose-6-phosphate dehydrogenase as an early marker of floral induction in shoot apices of Spinacia oleraceae var. Nobel. Plant Sci Lett 20: 109-113
14. Azaizeh H and Steudle E (1991) Effects of salinity on water Transport of excised maize (Zea mays L.) roots. Plant Physiol 97: 1136-1145
15. Balboni E (1978) A proline shuttle in insect flight muscle. Biochem Biophys Res Commun 85: 1090-1096
16. Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol. Plant 81: 563-570
17. Bassi R and Sharma SS (1993) Changes in proline content accompanying the uptake of zinc and copper by Lemna minor. Ann Bot 72: 151-154
18. Bellinger Y and Larher F (1987) Proline accumulation in higher plants: A redox buffer? Plant Physiol (Life Sci Adv.) 6: 23-27
19. Bernier G, Kinet J-M and Sachs R (1981) The Physiology of Flowering. Volume II. Transition to Reproductive Growth, pp 157-159. Boca Raton: CRC Press
20. Blake RL (1972) Animal model for hypoprolinaemia: Deficiency of mouse proline oxidase activity. Biochem J 129: 987-989
21. Blum A and Ebercon A (1976) Genotypic responses in sorghum to drought stress. III. Free proline accumulation and drought resistance. Crop Sci 16: 428-431
22. Blum A, Munns R, Passioura JB, Turner NC, Sharp RE, Boyer JS, Nguyen HT, Hsiao TC, Verma DPS and Hong Z (1996) Genetically engineered plants resistant to soil drying and salt stress: How to interpret osmotic relations? Plant Physiol 110: 1051-1053
23. Boggess SF, Koeppe DE and Stewart CR (1978) Oxidation of proline by plant mitochondria. Plant Physiol 62: 22-25
24. 1-pyrroline- 5-carboxylic acid dehydrogenase in barley, aproline-accumulating species. Plant Physiol 56: 259-262
25. Botha FC, Potgieter GP and Botha A-M (1992) Respiratory metabolism and gene expression during seed germination. Plant Growth Regul 11: 211-224
26. Bowman WD (1988) Ionic and water relation responses of two populations of a non-halophyte to salinity. J Exp Bot 39: 97-105
27. Boyer JS and Younis HM (1983) Molecular aspects of photosynthesis at low leaf water potentials. In: Marcelle R, Clijsters H and van Poucke M (eds) Effects of Stress on Photosynthesis, pp 29-33. The Hague: Martinus Nijhoff/Dr W. Junk Publishers
28. Branden C and Tooze J (1991) Introduction to Protein Structure. New York: Garland
29. 2 assimilation in oxygenic photosynthesis: The ferredoxin/thioredoxin system. Arch Biochem Biophys 288: 1-9
30. Cavalieri AJ and Huang AHC (1980) Carrier-protein- mediated transport of neutral amino acids into mung bean mitochondria. Plant Physiol 66: 588-591
31. Chandler PM and Robertson M (1994) Gene express ion regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45: 113-141
32. Chandler SF and Thorpe TA (1987) Characterisation of growth, water relations, and proline accumulation in sodium sulphate tolerant callus of Brassica napus L. cv Westar (Canola). Plant Physiol 84: 106-111
33. Chen SL and Kao CH (1995) Cd induced changes in proline level and peroxidase activity in roots of rice seedlings. Plant Growth Regul 17: 67-71
34. Chiang H-H and 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
35. Chou I,T Chen CT and Kao CH (1991) Characteristics of the induction of the accumulation of proline by abscisic acid and isobutyric acid in detached rice leaves. Plant Cell Physiol 32: 269-272
36. Chrominski A, Halls S, Weber DJ and Smith BN (1989) Proline affects ACC and ethylene conversion under salt and water stresses in the halophyte, Allenrolfea occidentalis. Environ Exp Bot 29: 359-363
37. Chu TM, Jusaitis M, Aspinall D and Paleg LG (1978) Accumulation of free proline at low temperatures. Physiol Plant 43: 254-260
38. 1-pyrroline-5-carboxylic acid reductase in Clostridium sporogenes. J Bacteriol 134: 139-146
39. Critchley C and Russell AW (1994) Photo inhibit ion of photosynthesis in vivo: The role of protein turnover in photosystem II. Physiol Plant 92: 188-196
40. Cruz RT, Jordan WR and Drew MC (1992) Structural changes and associated reduction of hydraulic conductance in roots of Sorghum bicolor L. following exposure to water deficit. Plant Physiol 99: 203-212
41. Dannehl H, Wietoska H, Heckmann H and Godde D (1996) Changes in D1-protein turnover and recovery of photosystem II activity precede accumulation of chlorophyll in plants after release from mineral stress. Planta 199: 34-42
42. Danon A and Mayfield SP (1994) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266: 1717-1719
43. 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol Gen Genet 221: 299-305
44. Delauney AJ and Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4: 215-223
45. Delauney AJ, Hu C-AA, Kavi Kishor PB and Verma DPS (1993) Cloning of ornithine-δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268: 18673-18678
46. Dietz K-J and Heilos L (1990) Carbon metabolism in spinach leaves as affected by leaf age and phosphorus and sulphur nutrition. Plant Physiol 93: 1219-1225
47. Dixon RA and Palva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085-1097
48. Doddema H, Eddin RS and Mahasneh A (1986) Effects of seasonal changes of soil and soil nitrogen on the N-metab olism of the halophyte Arthrocnemum fructicosum (L.) Moq. Plant Soil 92: 279
49. Draper SR (1972) Amino acid changes associated with low temperature Treatment of Lolium perenne. Phytochemistry 11: 639-641
50. Elthon TE and Stewart CR (1981) Submitochondrial location and electron transport characteristics of enzymes involved in proline oxidation. Plant Physiol 67: 780-784
51. Elthon TE and Stewart CR (1982) Proline oxidation in corn mitochondria: Involvement of NAD, relationship to ornithine metabolism: and sidedness of the inner membrane. Plant Physiol 70: 567-572
52. Elthon TE and Stewart CR (1984) Effects of the proline analogue L-thiazoline-4-carboxylic acid on proline metabolism. Plant Physiol 74: 213-218
53. Escoubas J-M, Lomas M, LaRoche J and Falkowski PG (1995) Light intensity regulates cab gene transcription via the redox state of the the plastoquinone pool in the green alga, Dunaliella tertiolecta. Proc Natl Acad Sci USA 92: 10237-10241
54. Fahrendorf T, Ni W, Shorrosh BS and Dixon RA (1995) Stress responses in alfalfa (Medicago sativa L.) XIX. Transcriptional activation of oxidative pentose phosphate pathway genes at the onset of the isoflavonoid phytoalexin response. Plant Mol Biol 28: 885-900
55. Finkelstein RR and Somerville CR (1990) Three classes of abscisic acid (ABA)-insensitive mutations of Arabidopsis define genes that control overlapping subsets of ABA responses. Plant Physiol 94: 1172-1179
56. Floyd RA and 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
57. Forsthoefel NR, Vernon DM and Cushman JC (1995) A salinity-induced gene from the halophyte M. crystallinum encodes a glycolytic enzyme, cofactor-independent phosophoglyceromutase. Plant Mol Biol 29: 213-226
58. Fricke W and Pahlich E (1990) The effect of water stress on the vacuole-extravacuole compartmentation of proline in potato cell suspension cultures. Physiol Plant 78: 374-378
59. Frommer WB, Hummel S and Riesmeier JW (1993) Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc Natl Acad Sci USA 90: 5944-5948
60. Fry IV, Huflejt M, Erber WWA, Peschek GA and Packer L (1986) The role of respiration during adaptation of the freshwater cyanobacterium Synechococcus 6311 to salinity. Arch Biochem Biophys 244: 686-691
61. Fryer MJ, Oxborough K, Martin B, Ort DR and Baker NR (1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Physiol 108: 761-767
62. Gäde G (1992) The hormonal integration of insect flight metabolism. Zool Jb Physiol 96: 211-225
63. Garcia AB, Engler AJ, Van Montagu M. and Caplan A (1993) Effect of NaCl and osmoprotectants on growth inhibition, ion accumulation, and gene expression in rice (Oryza sativa). In: Close TJ and Bray EA (eds) Plant Responses to Cellular Dehydration During Environmental Stress: pp 272-273. American Society of Plant Physiologists
64. Giardi MT, Cona A, Geiken B, Kučera T, Masojidek J and Mattoo AK (1996) Long-term drought stress induces structural and functional reorganisation of photosystem II. Planta 199: 118-125
65. Girousse C, Bournoville R and Bonnemain J-L (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiol 111: 109-113
66. Goas G, Goas M and Larher F (1982) Accumulation of free proline and glycine betaine in Aster tripolium subjected to a saline shock: A kinetic study related to light period. Physiol Plant 55: 383-388
67. 2 fumigation and recovery. Environ Pollu 7: 25-38
68. Göring H and Thien BH (1979) Influence of nutrient deficiency on proline accumulation in the cytoplasm of Zea mays L. seedlings. Biochem Physiol Pflanzen 174: 9-16
69. Gottlieb ML and Bray EA (1991) The induction of free proline accumulation by endogenous ABA in Arabidopsis thaliana during drought. Plant Physiol (suppl.) 96: S-21
70. Gray GR, Savitch LV, Ivanov AG and Huner NPA (1996) Photosystem II excitation pressure and the development of resistance to photo inhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110: 61-71
71. Greenway H and Setter TL (1979) Accumulation of proline and sucrose during the first hours after transfer of Chlorella emersonii to high NaCl. Aust J Plant Physiol 6: 69-79
72. Handa S, Handa AK, Hasegawa PM and Bressan RA (1986) Proline accumulation and the adaptation of cultured plant cells to salinity stress. Plant Physiol 80: 938-945
73. Hanson AD and Tully RE (1979) Light stimulation of proline synthesis in water-stressed barley leaves. Planta 145: 45-51
74. Hanukoglu I and Gutfinger T (1989) cDNA sequence of adrenodoxin reductase: Identification of NADP-binding sites in oxidoreductases. Eur J Biochem 180: 479-484
75. 1-pyrroline-5-carboxylate reductase in Arabidopsis thaliana. Plant Growth Regul 19: 249-256
76. Hare PD, Du Plessis S, Cress WA and Van Staden J (1996) Stress-induced changes in plant gene expression: Prospects for enhancing agricultural productivity in Southern Africa. S Afr J Sci 92: 431-439
77. Havaux M (1992) Stress tolerance of photosystem II in vivo: Antagonistic effects of water, heat, and photo inhibition stresses. Plant Physiol 100: 424-432
78. Hayward DC, Delaney SJ, Campbell HD, Ghysen A, Benzer S, Kasprzak AB, Cotsell JN, Young IG. and 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
79. Hayzer DJ and Leisinger Th (1980) The gene-enzyme relationships of proline biosynthesis in Escherichia coli. J Gen Microbiol 118: 287-293
80. He JX, Wang J and Liang HG (1995) Effects of water stress on photochemical function and protein metabolism of photosystem II in wheat leaves. Physiol Plant 93: 771-777
81. Hellebust JA and Larochelle J (1988) Compartmentation and activities of enzymes involved in the metabolism of amino acids implicated in osmoregulatory mechanisms in Acanthamoeba castellanii. J Protozool 35: 498-502
82. Herbers K, Meuwly P, Frommer WB, Métraux J-P and Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: Possible hexose sensing in the secretory pathway. Plant Cell 8: 793-803
83. Hervieu F, Le Dily F, Huault C and Billard J-P (1995) Contribution of ornithine aminotransferase to proline accumulation in NaCl-treated radish cotyledons. Plant Cell Environ 18: 205-210
84. Heuer B (1994) Osmoregulatory role of proline in water and salt-stressed plants. In: Pessarakli M (ed) Handbook of Plant and Crop Stress, pp 363-381. New York: Marcel Dekker, Inc
85. Hodgson RAJ and Raison JK (1989) Inhibition of photosynthesis by chilling in moderate light: A comparison of plants sensitive and insensitive to chilling. Planta 178: 545-552
86. 1-pyrroline-5-carboxylate synthetase) catalyses the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89: 9345-9358
87. Huang AHC and Cavalieri AJ (1979) Proline oxidase and water stress-induced proline accumulation in spinach leaves. Plant Physiol 63: 531-535
88. Huner NPA, Gunnar O, Hurry VM, Krol M, Falk S and Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37: 19-39
89. Itai C and Paleg LG (1982) Responses of water-stressed Hordeum distichum L. and Cucumis sativus to proline and betaine. Plant Sci Lett 25: 329-335
90. Jang J-C and Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665-1679
91. Jeanjean R, Matthijs HCP, Onana B, Havaux M and Joset F (1993) Exposure of the cyanobacterium Synechcystis PCC 6803 to salt stress induces concerted changes in respiration and photosynthesis. Plant Cell Physiol 34: 1073-1079
92. Joshi SS (1984) Effect of salinity stress on organic and mineral constituents in the leaves of pigeonpea (Cajanus cojan L. var. C-11) Plant Soil 82: 69-75
93. Jost A, Perlman S, Valentino O, Castanier M, Scoller R and Marge S (1988) Experimental control of differentiation of Leydig cells in the rat fetal testis. Proc Natl Acad Sci USA 85: 8094-8097
94. Kandpal RP and Rao NA (1985) Alterations in the biosynthesis of proteins and nucleic acids in finger millet (Eleucine corocana) seedlings during water stress and the effect of proline on protein biosynthesis. Plant Sci 40: 73-79
95. 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108: 1387-1394
96. Kohl DH, Lin JJ, Shearer G and Schubert KR (1990) Activities of the pentose phosphate pathway and enzymes of proline metabolism in legume root nodules. Plant Physiol 94: 1258- 1264
97. 2-fixing root nodules: Energy transfer and regulation of purine synthesis. Proc Natl Acad Sci USA 85: 2036-2040
98. 2 reducing) activity and activities of enzymes related to proline metabolism in drought-stressed soybean nodules. J Exp Bot 240: 831-837
99. Krackhardt M and Guerrier G (1995) Effect of osmotic and ionic stresses on proline and organic acid contents during imbibition and germination of soybean seeds. J Plant Physiol 146: 725-730
100. Krueger R, Jäger H-J, Hintz M and Pahlich E (1986) Purification to homogeneity of pyrroline-5-carboxy late reductase of barley. Plant Physiol 80: 142-144
101. Kuo CG and Chen BW (1980) Physiological responses of tomato cultivars to flooding. J Am Soc Hort Sci 105: 751- 755
102. Kuo CG, Chen HM and Ma LH (1986) Effect of high temperature on proline content in tomato floral buds and leaves. J Am Soc Hort Sci 111: 746-750
103. Kurkdjian A and Guern J (1989) Intracellular pH: Measurement and importance in cell activity. Annu Rev Plant Physiol 40: 271-303
104. Labanauskas CK, Stolzy LH and Handy MF (1974) Soil oxygen and Phytophthera spp. root infestation effects on protein and free amino acids in lemon and orange leaves. J Am Soc Hort Sci 99: 497-500
105. Lagrimini LM, Burkhart W, Moyer M and Rothstein S (1987) Molecular cloning of complementary DNA encoding the lignin forming peroxidase from tobacco: Molecular analysis and tissue specific expression. Proc Natl Acad Sci USA 84: 7542-75466
106. 1-pyrroline-5-carboxylate reductase. Plant Physiol 96: 245-250
107. Lawlor DW and Uprety DC (1993) Effects of water stress on photosynthesis of crops and the biochemical mechanism. In: Abrol YP, Mohanty P and Govindjee (eds) Photosynthesis: Photoreactions to Plant Productivity pp 419-449. Dordrecht: Kluwer
108. Laxalt MA, Cassia RO, Sanllorenti PM, Madrid EA, Andreu AB, Daleo GR, Conde RD and Lamattina L (1996) Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol Biol 30: 961-972
109. Leigh RA, Ahmad N and Wyn Jones RG (1981) Assessment of glycinebetaine and proline compartmentation by analysis of isolated beet vacuoles. Planta 153: 34-41
110. Levings CS III and Siedow JN (1995) Regulation of redox poise in chloroplasts. Science 268: 695-696
111. Leyva A, Jarillo JA, Salinas J and Martinez-Zapater J (1995) Low temperature induces the accumulation of phenylalanine ammonia-lyase and chalcone synthase mRNAs of Arabidopsis thaliana in a light-dependent manner. Plant Physiol 108: 39-46
112. Lutz C, Steiger A and Godde D (1992) Influence of air pollutants and nutrient deficiency on D-1 protein content and photosynthesis in young spruce trees. Physiol Plant 85: 611- 617
113. Madan S, Nainawatee HS, Jain RK and Chowdhury JB (1995) Proline and proline metabolising enzymes in in vitro selected NaCl-tolerant Brassica juncea L. under salt stress. Ann Bot 76: 51-57
114. Maxwell DP, Falk S and Huner NPA (1995a) Photosystem II excitation pressure and the development of resistance to photoinhibition. I. LHCII abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107: 687-694
115. Maxwell DP, Laudenbach DE and Huner NPA (1995b) Redox regulation of light-harvesting complex II and cab mRNA abundance in Dunaliella salina. Plant Physiol 109: 787-795
116. Melo-Oliveira R, Oliveira IC and Coruzzi GM (1996) Arabidopsis mutant analysis and gene regulation define a nonredundant role for glutamate dehydrogenase in nitrogen assimilation. Proc Natl Acad Sci USA 93: 4718-4723
117. Meon S, Fisher JM and Wallace HR (1978) Changes in free proline following infection of plants with either Meloidogyne javanica or Agrobacterium tumefaciens. Physiol Plant Pathol 12: 251-256
118. Mohanty SK and Sridhar R (1982) Physiology of rice tungro virus disease: Proline accumulation due to infection. Physiol Plant 56: 89-93
119. Mumtaz S, Naqvi SSM, Shereen A and Khan MA (1995) Proline accumulation in wheat seedlings subjected to various stresses. Acta Physiol Plant 17: 17-20
120. Naidu BP, Paleg LG, Aspinall D, Jennings AC and Jones GP (1990) Rate of imposition of water stress alters the accumulation of nitrogen-containing solutes by wheat seedlings. Aust J Plant Physiol 17: 653-664
121. Naidu BP, Paleg LG, Aspinall D, Jennings AC and Jones GP (1991) Amino acid and glycine betaine accumulation in cold-stresssed wheat seedlings. Phytochemistry 30: 407-409
122. Naik GP and Joshi GV (1983) Ineffectual role of proline metabolism in salt-stressed sugarcane leaves. Proc Indian Acad Sci 92: 265-272
123. Niu X, Bressan RA, Hasegawa PM and Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109: 735-742
124. 2 assimilation in pea leaves on exposure to UV-B radiation. Plant Cell Environ 18: 781-787
125. Nonami H and Boyer JS (1990) Wall extensibility and cell hydraulic conductivity decrease in enlarging stem tissues at low water potentials. Plant Physiol 93: 1610-1619
126. Ober ES and Sharp RE (1994) Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. I. Requirement for increased levels of abscisic acid. Plant Physiol 105: 981-987
127. O'Regan BP, Cress WA and van Staden J (1993) Root growth, water relations, abscisic acid and proline levels of drought- resistant and drought-sensitive maize cultivars in response to water stress. S Afr J Bot 59: 98-104
128. Pahlich E, Kerres R and Jäger H-J (1983) Influence of water stress on the vacuole/extravacuole distribution of proline in protoplasts of Nicotiana rustica. Plant Physiol 72: 590-591
129. Pardha Saradhi P, Alia, Arora S and Prasad KVSK (1995) Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem Biophys Res Commun 209: 1-5
130. Perino C and Come D (1991) Physiological and metabolical study of the germination phases in apple embryo. Seed Sci Technol 19: 1-14
131. Pesci P (1993) Glucose mimics the enhancing effect of light on ABA-induced proline accumulation inhydrated barley and wheat leaves. J Plant Physiol 142: 355-359
132. Phang JM (1985) The regulatory functions of proline and pyrroline-5-carboxylic acid. Curr Top Cell Regul 25: 91-132
133. Portis AR (1992) Regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase activity. Annu Rev Plant Physiol Plant Mol Biol 43: 415-437
134. Pryke JA and Ap Rees T (1976) Activity of the pentose phosphate pathway during lignification. Planta 132: 279-284
135. Pryke JA and Ap Rees T (1977) The pentose phosphate pathway as a source of NADPH for lignin synthesis. Phytochemistry 16: 557-560
136. Rayapati PJ and Stewart CR (1991) Solubilisation of a proline dehydrogenase from maize (Zea mays L.) mitochondria. Plant Physiol 95: 787-791
137. Rayapati PJ, Stewart CR and Hack E (1989) Pyrroline-5- carboxylate reductase is in pea (Pisum sativum L.) leaf chloroplasts. Physiol Plant 91: 581-586
138. Rob M, Roelfsema G, Hidde B and Prins A (1995) Effect of absicisic acid on stomatal opening in isolated epidermal stips of abi mutants of Arabidopsis thaliana. Physiol Plant 95: 373-378
139. Robertson D, Davies DR, Gerish C, Jupe SC and Bolwell GP (1995) Rapid changes in oxidative metabolism as a consequence of elicitor treatment of suspension-cultured cells of French bean (Phaseolus vulgaris L.) Plant Mol Biol 27: 59-67
140. Rodriguez MM and Heyser JW (1988) Growth inhibition by exogenous proline and its metabolism in saltgrass (Distichlis spicata) suspension cultures. Plant Cell Rep 7: 305-311
141. Rudolph AS, Crowe JH and Crowe LM (1986) Effects of three stabilising agents - proline, betaine and trehalose - on membrane phospholipids. Arch Biochem Biophys 245: 134- 143
142. Sanada Y, Ueda H, Kuribayashi K, Andoh T, Hayashi F, Tamai N and Wada K (1995) Novel light-dark change of proline levels in halophyte (Mesembryanthemum crystallinum L.) and glycophytes (Hordeum vulgare L. and Titicum aestivum L.) leaves and roots under salt stress. Plant Cell Physiol 36: 965-970
143. Savitch LV, Maxwell DP and Huner NPA (1996) Photosystem II excitation pressure and photosynthetic carbon metabolism in Chlorella vulgaris. Plant Physiol 111: 127-136
144. 1-pyrroline- 5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett 372: 13-19
145. Schobert B and Tschesche H (1978) Unusual solution properties of proline and its interactions with proteins. Biochem Biophys Acta 541: 270-277
146. Seitz EW and Hochster RM (1964) Free proline in normal and in crown-gall tumour tissue of tomato and tobacco. Life Sci 3: 1033-1037
147. Sells GD and Koeppe DE (1981) Oxidation of proline by mitochondria isolated from water-stressed maize shoots. Plant Physiol 68: 1058-1063
148. Shetty K, Shetty GA, Nakazakim Y, Yoshioka Y, Asano, Y. and Oosawa K (1992) Stimulation of benzyladenine-induced in vitro shoot organogenesis in Cucumis melo L. by proline, salicylic acid and aspirin. Plant Sci 84: 193-199
149. Skubatz H, Meeuse BJD and Bendich AJ (1989) Oxidation of proline and glutamate by mitochondria of the inflorescence of voodoo lily (Sauromatum guttatum). Plant Physiol 91: 530- 535
150. Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125: 27-58
151. Smirnoff N and Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28: 1057-1060
152. Stewart CR (1978) Role of carbohydrates in proline accumulation in wilted barley leaves. Plant Physiol 61: 775-778
153. Stewart CR and Boggess SF (1977) The effect of wilting on the conversion of arginine, ornithine: and glutamate to proline in bean leaves. Plant Sci Lett 8: 147-153
154. 1-pyrroline-5-carboxylic acid dehydrogenase in mitochondrial preparations from plant seedlings. Plant Sci Lett 3: 173-181
155. Stewart CR and Lee JA (1974) The role of proline accumulation inhalophytes. Planta 120: 279-289
156. Stewart CR and Voetberg G (1985) Relationship between stress-induced ABA and proline accumulations and ABA- induced proline accumulation in excised barley leaves. Plant Physiol 79: 24-27
157. Stewart CR, Boggess SF, Aspinall D and Paleg LG (1977) Inhibition of proline oxidation by water stress. Plant Physiol 59: 930-932
158. Storey R and Wyn Jones RG (1977) Quaternary ammonium compounds in plants in relation to salt resistance. Phytochemistry 16: 447
159. 1-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean. Plant Physiol 99: 1642-1649
160. Taylor AA and Stewart CR (1981) Tissue and subcellular localisation of enzymes of arginine metabolism in Pisum sativum. Biochem Biophys Res Commun 101: 1281-1289
161. Timpa JD, Burke JJ, Quisenberry JE and Wendt CW (1986) Effects of water stress on the organic acid and carbohydrate composition of cotton plants. Plant Physiol 82: 724-728
162. Vance CP, Kirk TK and Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18: 259-288
163. Van Rensburg L, Krüger GHJ and Krüger H (1993) Proline accumulation as drought tolerance selection criterion: Its relationship to membrane integrity and chloroplast ultrastructure in Nicotiana tabacum L. J Plant Physiol 141: 188-194
164. Van Swaaij AC, Jacobsen E and Feenstra WJ (1985) Effect of cold hardening, wilting and exogenously applied proline on leaf proline content and frost tolerance of several genotypes of Solanum. Physiol Plant 64: 230-236
165. Vassiliev IR, Kolber Z, Wyman KD, Mauzerall D, Shukla VK and Falkowski PG (1995) Effects of iron limitation on photosystem II composition and light utilisation in Dunaliella tertiolecta. Plant Physiol 109: 963-972
166. Vaucheret H, Kronenberger J, Lepingle A, Vilaine F, Boutin J-P and Caboche M (1992) Inhibition of tobacco nitrite reductase activity by expression of antisense RNA. Plant J 2: 559- 569
167. Venekamp JH (1989) Regulation of cytosol acidity in plants under conditions of drought. Physiol Plant 76: 112-117
168. Verbruggen N, Villarroel R and Van Montagu M (1993) Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol 103: 771-781
169. Voetberg GS and Sharp RE (1991) Growth of the maize primary root at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol 96: 125-130
170. Von Schaewen A, Lagenkämper G, Graeve K, Wenderoth I and Scheibe R (1995) Molecular characterisation of the plastidic glucose-6-phosphate dehydrogenase from potato in comparison to its cytosolic counterpart. Plant Physiol 109: 1327-1335
171. Wakabayashi Y, Yamada E, Hasegawa T and Yamada R-H (1991) Enzymological evidence for the indispensability of small intestine in the synthesis of arginine from glutamate. I. Pyrroline-5-carboxylate synthase. Arch Biochem Biophys 291: 1-8
172. Walton EF, Clark CJ and Boldingh HL (1991) Effect of hydrogen cyanamide onamino acid profiles in kiwifruit buds during budbreak. Plant Physiol 97: 1256-1259
173. Wang S-S and Brandriss MC (1987) Proline utilisation in Saccharomyces cerevisiae: Analysis of the cloned PUT1 gene product. Mol Cell Biol 7: 4431-4440
174. Werner JE and Finkelstein RR (1995) Arabidopsis mutants with reduced response to NaCl and osmotic stress. Physiol Plant 93: 659-666
175. 1-pyrroline-5- carboxylate reductase (proC) gene in pea (Pisum sativum L.). Plant Physiol 100: 1464-1470
176. Wrench P, Wight L, Brady CJ and Hinde RW (1977) The source of carbon for proline synthesis in osmotically stressed artichoke tuber slices. Aust J Plant Physiol 4: 7033-711
177. Yang Y, Kwon H-B, Peng H-P and Shih M-C (1993) Stress responses and metabolic regulation of glyceraldehyde-3- phosphate dehydrogenase genes in Arabidopsis. Plant Physiol 101: 209-216
178. Yeh GC and Phang JM (1988) Stimulation of phosphoribosyl pyrophosphate and purine nucleotide production by pyrroline-5-carboxylate inhuman erythrocytes. J Biol Chem 263: 13083-13089
179. 1- pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. Plant J 7: 751-760