Evolution of proline biosynthesis: Enzymology, bioinformatics, genetics, and transcriptional regulation

Biological Reviews

Volumn 90, Issue 4, 2015, Pages 1065-1099

  Fichman, Yosef ^a   Gerdes, Svetlana Y ^b   Kovács, Hajnalka ^c   Szabados, László ^c   Zilberstein, Aviah ^a   Csonka, Laszlo N ^d  

^a TEL AVIV UNIVERSITY   (Israel)

^b ARGONNE NATIONAL LABORATORY   (United States)

^c INSTITUTE OF BIOCHEMISTRY   (Hungary)

^d PURDUE UNIVERSITY   (United States)

Author keywords

Ornithine aminotransferase; Osmotic stress; Proline; glutamyl kinase; glutamyl phosphate reductase; 1 pyrroline 5 carboxylate reductase; 1 pyrroline 5 carboxylate synthase

Indexed keywords

PROLINE;

ARCHAEON; BACTERIUM; BIOSYNTHESIS; EUKARYOTE; EVOLUTION; GENE EXPRESSION REGULATION; METABOLISM;

ARCHAEA; BACTERIA; BIOLOGICAL EVOLUTION; EUKARYOTA; GENE EXPRESSION REGULATION; PROLINE;

EID: 84943419982     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12146     Document Type: Article

References (244)

1. Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2003). Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15, 63-78.
2. Ábrahám, E., Rigó, G., Székely, 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 Molecular Biology 51, 363-372.
3. Agarwal, P., Reddy, M. P. & Chikara, J. (2011). WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Molecular Biology Reports 38, 3883-3896.
4. Aravind, L. & Koonin, E. V. (1999). Novel predicted RNA-binding domains associated with the translation machinery. Journal of Molecular Evolution 48, 291-302.
5. Ashkenazy, H., Erez, E., Martz, E., Pupko, T. & Ben-Tal, N. (2010). ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Research 38, W529-W533.
6. 1-pyrroline-5-carboxylate synthase. Human Molecular Genetics 9, 2853-2858.
7. 1-pyrroline-5-carboxylate synthase deficiency: neurodegeneration, cataracts and connective tissue manifestations combined with hyperammonaemia and reduced ornithine, citrulline, arginine and proline. European Journal of Pediatrics 164, 31-36.
8. Belitsky, B. R., Brill, J., Bremer, E. & Sonenshein, A. L. (2001). Multiple genes for the last step of proline biosynthesis in Bacillus subtilis. Journal of Bacteriology 183, 4389-4392.
9. Berezin, C., Glaser, F., Rosenberg, J., Paz, I., Pupko, T., Fariselli, P., Casadio, R. & Ben-Tal, N. (2004). ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics 20, 1322-1324.
10. Berg, C. M. & Rossi, J. J. (1974). Proline excretion and indirect suppression in Escherichia coli and Salmonella typhimurium. Journal of Bacteriology 118, 928-934.
11. 1-pyrroline-5-carboxylate synthase (P5CS), causes an autosomal recessive neurocutaneous syndrome. European Journal of Human Genetics 16, 1176-1186.
12. Bloom, F., Smith, C. J., Jessee, J., Veilleux, B., Deutch, A. H., Downey, R. K., Ahmad, F. & Schultz, J. (1983). The use of genetically engineered strains of Escherichia coli for the overproduction of free amino acids: proline as a a model system. In Advances in Gene Technology: Molecular Genetics of Plants and Animals, pp. 383-394. Academic Press, Orlando.
13. Blum, A., Munns, R., Passioura, J. B., Turner, N. C., Sharp, R. E., Boyer, J. S., Nguyen, H. T., Hsiao, T. C., Verma, D. & Hong, Z. (1996). Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations? Plant Physiology 110, 1051-1053.
14. Boccazzi, P., Zanzotto, A., Szita, N., Bhattacharya, S., Jensen, K. & Sinskey, A. (2005). Gene expression analysis of Escherichia coli grown in miniaturized bioreactor platforms for high-throughput analysis of growth and genomic data. Applied Microbiology and Biotechnology 68, 518-532.
15. Bouchabke-Coussa, O., Quashie, M.-L., Seoane-Redondo, J., Fortabat, M.-N., Gery, C., Yu, A., Linderme, D., Trouverie, J., Granier, F., Teoule, E. & Durand-Tardif, M. (2008). ESKIMO1 is a key gene involved in water economy as well as cold acclimation and salt tolerance. BMC Plant Biology 8, 125, doi: 10.1186/1471-2229-8-125.
16. Brady, R. A. & Csonka, L. N. (1988). Transcriptional regulation of the proC gene of Salmonella typhimurium. Journal of Bacteriology 170, 2379-2382.
17. Brill, J., Hoffmann, T., Putzer, H. & Bremer, E. (2011). T-box-mediated control of the anabolic proline biosynthetic genes of Bacillus subtilis. Microbiology 157, 977-987.
18. Brinkman, F. S., Blanchard, J. L., Cherkasov, A., Av-Gay, Y., Brunham, R. C., Fernandez, R. C., Finlay, B. B., Otto, S. P., Ouellette, B. F., Keeling, P. J., Rose, A. M., Hancock, R. E., Jones, S. J. & Greberg, H. (2002). Evidence that plant-like genes in Chlamydia species reflect an ancestral relationship between Chlamydiaceae, cyanobacteria, and the chloroplast. Genome Research 12, 1159-1167.
19. Buxton, R. S. (1980). Selection of Bacillus subtilis 168 mutants with deletions of the pbsx prophage. Journal of General Virology 46, 427-437.
20. Cao, S., Cai, Y., Yang, Z. & Zheng, Y. (2012). MeJA induces chilling tolerance in loquat fruit by regulating proline and γ-aminobutyric acid contents. Food Chemistry 133, 1466-1470.
21. Casalino, L., Comes, S., Lambazzi, G., De Stefano, B., Filosa, S., De Falco, S., De Cesare, D., Minchiotti, G. & Patriarca, E. J. (2011). Control of embryonic stem cell metastability by L-proline catabolism. Journal of Molecular Cell Biology 3, 108-122.
22. Cayley, S., Lewis, B. A., Guttman, H. J. & Record, M. T. Jr. (1991). Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: implications for protein-DNA interactions in vivo. Journal of Molecular Biology 222, 281-300.
23. Cecchini, N. M., Monteoliva, M. I. & Alvarez, M. E. (2011). Proline dehydrogenase contributes to pathogen defense in Arabidopsis. Plant Physiology 155, 1947-1959.
24. Chattopadhyay, S., Ang, L. H., Puente, P., Deng, X. W. & Wei, N. (1998). Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10, 673-683.
25. Chen, M., Cao, J., Zheng, C. & Liu, Q. (2006). Directed evolution of an artificial bifunctional enzyme, γ-glutamyl kinase/γ-glutamyl phosphate reductase, for improved osmotic tolerance of Escherichia coli transformants. Federation of European Microbiological Societies Microbiology Letters 263, 41-47.
26. Chen, C. & Dickman, M. B. (2005). Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proceedings of the National Academy of Sciences of the United States of America 102, 3459-3464.
27. Chen, J. B., Wang, S. M., Jing, R. L. & Mao, X. G. (2009). Cloning the PvP5CS gene from common bean (Phaseolus vulgaris) and its expression patterns under abiotic stresses. Journal of Plant Physiology 166, 12-19.
28. Chen, H., Zhang, J., Neff, M. M., Hong, S. W., Zhang, H., Deng, X. W. & Xiong, L. (2008). Integration of light and abscisic acid signaling during seed germination and early seedling development. Proceedings of the National Academy of Sciences of the United States of America 105, 4495-4500.
29. Choi, H., Hong, J., Ha, J., Kang, J. & Kim, S. Y. (2000). ABFs, a family of ABA-responsive element binding factors. Journal of Biological Chemistry 275, 1723-1730.
30. Christian, J. H. B. (1955a). The influence of nutrition on the water relations of Salmonella oranienburg. Australian Journal of Biological Sciences 8, 75-82.
31. Christian, J. H. B. (1955b). The water relations of growth and respiration of Salmonella oranienburg at 30 °C. Australian Journal of Biological Sciences 8, 490-497.
32. Comes, S., Gagliardi, M., Laprano, N., Fico, A., Cimmino, A., Palamidessi, A., De Cesare, D., De Falco, S., Angelini, C., Scita, G., Patriarca, E. J., Matarazzo, M. R. & Minchiotti, G. (2013). L-proline induces a mesenchymal-like invasive program in embryonic stem cells by remodeling H3K9 and H3K36 methylation. Stem Cell Reports 1, 307-321.
33. Condamine, H. (1971). Proline production regulation in E. coli K 12. Annales de l'Institut Pasteur 120, 126-143.
34. Costilow, R. N. & Laycock, L. (1969). Reactions involved in the conversion of ornithine to proline in Clostridia. Journal of Bacteriology 100, 662-667.
35. Costilow, R. N. & Laycock, L. (1971). Ornithine cyclase (deaminating): purification of a protein that converts ornithine to proline and definition of the optimal assay conditions. Journal of Biological Chemistry 246, 6655-6660.
36. Csonka, L. N. (1981). Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Molecular and General Genetics MGG 182, 82-86.
37. Csonka, L. N. (1982). A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength. Journal of Bacteriology 151, 1433-1443.
38. Csonka, L. N. (1988). Regulation of cytoplasmic proline levels in Salmonella typhimurium: effect of osmotic stress on synthesis, degradation, and cellular retention of proline. Journal of Bacteriology 170, 2374-2378.
39. Csonka, L. N. & Fraenkel, D. G. (1977). Pathways of NADPH formation in Escherichia coli. Journal of Biological Chemistry 252, 3382-3391.
40. Csonka, L. N. & Leisinger, T. (2007). Biosynthesis of proline. In EcoSal-Escherichia coli and Salmonella: Cellular and Molecular Biology. (eds A . Böck, R . Curtis III, J. B . Kaper, R. D . Karp, F. C . Neidhardt, T . Nystrom, K. E . Rudd, and C. L . Squires). Chapter 34.6.1.4. ASM Press. Washington, D. C. Electronic edition. doi: 10.1128/ecosal.4.7.4.
41. Dandekar, A. M. & Uratsu, S. L. (1988). A single base pair change in proline biosynthesis genes causes osmotic stress tolerance. Journal of Bacteriology 170, 5943-5945.
42. De Ingeniis, J., Ratnikov, B., Richardson, A. D., Scott, D. A., Aza-Blanc, P., De, S. K., Kazanov, M., Pellecchia, M., Ronai, Z., Osterman, A. L. & Smith, J. W. (2012). Functional specialization in proline biosynthesis of melanoma. PLoS One 7, e45190.
43. Delauney, A. J., Hu, C. A., Kishor, P. B. & Verma, D. P. (1993). Cloning of ornithine δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. Journal of Biological Chemistry 268, 18673-18678.
44. 1-pyrroline-5-carboxylate reductase was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Molecular and General Genetics MGG 221, 299-305.
45. Delauney, A. J. & Verma, D. P. S. (1993). Proline biosynthesis and osmoregulation in plants. The Plant Journal 4, 215-223.
46. Dessaux, Y., Petit, A., Tempé, J., Demarez, M., Legrain, C. & Wiame, J. M. (1986). Arginine catabolism in Agrobacterium strains: role of the Ti plasmid. Journal of Bacteriology 166, 44-50.
47. 1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16, 3413-3425.
48. Deutch, A. H., Rushlow, K. E. & Smith, C. J. (1984). Analysis of the Escherichia coli proBA locus by DNA and protein sequencing. Nucleic Acids Research 12, 6337-6355.
49. 1-pyrroline-5-carboxylate reductase: gene sequence, protein overproduction and purification. Nucleic Acids Research 10, 7701-7714.
50. Dietz, K. J., Vogel, M. & Viehhauser, A. (2010). AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245, 3-14.
51. Dubouzet, J. G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E. G., Miura, S., Seki, M., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2003). OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal 33, 751-763.
52. Ernst, T., Hergenhahn, M., Kenzelmann, M., Cohen, C. D., Bonrouhi, M., Weninger, A., Klären, R., Gröne, E. F., Wiesel, M., Güdemann, C., Küster, J., Schott, W., Staehler, G., Kretzler, M., Hollstein, M. & Gröne, H. J. (2002). Decrease and gain of gene expression are equally discriminatory markers for prostate carcinoma: a gene expression analysis on total and microdissected prostate tissue. American Journal of Pathology 160, 2169-2180.
53. Fabro, G., Kovács, I., Pavet, V., Szabados, L. & Alvarez, M. E. (2004). Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Molecular Plant-Microbe Interactions 17, 343-350.
54. Foster, R., Izawa, T. & Chua, N. H. (1994). Plant bZIP proteins gather at ACGT elements. The Federation of American Societies for Experimental Biology Journal 8, 192-200.
55. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.-Y., Cutler, S. R., Sheen, J., Rodriguez, P. L. & Zhu, J. K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660-664.
56. 1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiology 118, 661-674.
57. Fujita, T., Maggio, A., Garci{dotless}a-Ri{dotless}os, M., Stauffacher, C., Bressan, R. A. & Csonka, L. N. (2003). Identification of regions of the tomato γ-glutamyl kinase that are involved in allosteric regulation by proline. Journal of Biological Chemistry 278, 14203-14210.
58. Funck, D., Stadelhofer, B. & Koch, W. (2008). Ornithine-δ-aminotransferase is essential for arginine catabolism but not for proline biosynthesis. BMC Plant Biology 8, 40, doi: 10.1186/1471-2229-8-40.
59. Funck, D., Winter, G., Baumgarten, L. & Forlani, G. (2012). Requirement of proline synthesis during Arabidopsis reproductive development. BMC Plant Biology 12, 191. doi: 10.1186/1471-2229-12-19.
60. Fyhn, H. J. (1976). Holeuryhalinity and its mechanisms in a cirriped crustacean, Balanus improvisus. Comparative Biochemistry and Physiology. Part A, Physiology 53, 19-30.
61. Garrett, M. A. & Bradley, T. J. (1987). Extracellular accumulation of proline, serine and trehalose in the haemolymph of osmoconforming brackish-water mosquitoes. Journal of Experimental Biology 129, 231-238.
62. Gilles, R. & Schoffeniels, E. (1969). Isosmotic regulation in isolated surviving nerves of eriocheir sinensis Milne Edwards. Comparative Biochemistry and Physiology 31, 927-939.
63. 1-pyrroline-5-carboxylate synthase in alfalfa, transcriptionally induced upon salt stress. Plant Molecular Biology 38, 755-764.
64. 1-pyrroline-2-carboxylate reductase belonging to a new family of NAD(P)H-dependent oxidoreductases: conformational change, substrate recognition, and stereochemistry of the reaction. Journal of Biological Chemistry 280, 40875-40884.
65. Graupner, M. & White, R. H. (2001). Methanococcus jannaschii generates L-proline by cyclization of L-ornithine. Journal of Bacteriology 183, 5203-5205.
66. Gu, L., Liu, Y., Zong, X., Liu, L., Li, D.-P. & Li, D.-Q. (2010). Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Molecular Biology Reports 37, 4067-4073.
67. Guernsey, D. L., Jiang, H., Evans, S. C., Ferguson, M., Matsuoka, M., Nightingale, M., Rideout, A. L., Provost, S., Bedard, K., Orr, A., Dubé, M. P., Ludman, M. & Samuels, M. E. (2009). Mutation in pyrroline-5-carboxylate reductase 1 gene in families with cutis laxa type 2. American Journal of Human Genetics 85, 120-129.
68. Hahne, H., Mäder, U., Otto, A., Bonn, F., Steil, L., Bremer, E., Hecker, M. & Becher, D. (2010). A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. Journal of Bacteriology 192, 870-882.
69. Hao, D., Ohme-Takagi, M. & Yamasaki, K. (2003). A modified sensor chip for surface plasmon resonance enables a rapid determination of sequence specificity of DNA-binding proteins. The Federation of European Biochemical Societies Letters 536, 151-156.
70. Hao, D., Yamasaki, K., Sarai, A. & Ohme-Takagi, M. (2002). Determinants in the sequence specific binding of two plant transcription factors, CBF1 and NtERF2, to the DRE and GCC motifs. Biochemistry 41, 4202-4208.
71. Hare, P. D. & Cress, W. A. (1997). Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79-102.
72. Haudecoeur, E., Planamente, S., Cirou, A., Tannières, M., Shelp, B. J., Moréra, S. & Faure, D. (2009). Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences of the United States of America 106, 14587-14592.
73. Hayashi, F., Ichino, T., Osanai, M. & Wada, K. (2000). Oscillation and regulation of proline content by P5CS and ProDH gene expressions in the light/dark cycles in Arabidopsis thaliana L. Plant and Cell Physiology 41, 1096-1101.
74. Hayzer, D. J. & Leisinger, T. (1980). The gene-enzyme relationships of proline biosynthesis in Escherichia coli. Journal of General Microbiology 118, 287-293.
75. Hayzer, D. J. & Leisinger, T. (1982). Proline biosynthesis in Escherichia coli. European Journal of Biochemistry 121, 561-565.
76. Hayzer, D. J. & Leisinger, T. (1983). Proline biosynthesis in Escherichia coli kinetic and mechanistic properties of glutamate semialdehyde dehydrogenase. Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology 742, 391-398.
77. Hayzer, D. J. & Moses, V. (1978). The enzymes of proline biosynthesis in Escherichia coli. Their molecular weights and the problem of enzyme aggregation. The Biochemical Journal 173, 219-228.
78. He, X., Hou, X., Shen, Y. & Huang, Z. (2011). TaSRG, a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis. The Federation of European Biochemical Societies Letters 585, 1231-1237.
79. Hehl R. & Bülow L. (2014). Athamap web tools for the analysis of transcriptional and posttranscriptional regulation of gene expression in Arabidopsis thaliana. Methods in Molecular Biology 1158, 139-156.
80. Hellmann, H., Funck, D., Rentsch, D. & Frommer, W. B. (2000). Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiology 123, 779-789.
81. Hernandez, P., Ordoñez, J. & Sanz Perez, B. (1983). Use of the Mud(Ap, lac) bacteriophage to study the regulation of L-proline biosynthetic genes in Escherichia coli K-12. Current Microbiology 9, 31-35.
82. Hoffmann, T., von Blohn, C., Stanek, A., Moses, S., Barzantny, H. & Bremer, E. (2012). Synthesis, release, and recapture of compatible solute proline by osmotically stressed Bacillus subtilis cells. Applied and Environmental Microbiology 78, 5753-5762.
83. 1-1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology 122, 1129-1136.
84. 1-1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of the National Academy of Sciences of the United States of America 89, 9354-9358.
85. 1-pyrroline-5-carboxylate synthase: function and regulation. Amino Acids 35, 665-672.
86. 1-pyrroline-5-carboxylate synthase: alternative splice donor utilization generates isoforms with different sensitivity to ornithine inhibition. Journal of Biological Chemistry 274, 6754-6762.
87. Huh, S. M., Noh, E. K., Kim, H. G., Jeon, B. W., Bae, K., Hu, H. C., Kwak, J. M. & Park, O. K. (2010). Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt stress responses. Plant and Cell Physiology 51, 1499-1514.
88. Hur, J., Jung, K. H., Lee, C. H. & An, G. (2004). Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Science 167, 417-426.
89. 1-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.
90. Inamine, G. S. & Dubnau, D. (1995). ComEA, a Bacillus subtilis integral membrane protein required for genetic transformation, is needed for both DNA binding and transport. Journal of Bacteriology 177, 3045-3051.
91. Inana, G., Totsuka, S., Redmond, M., Dougherty, T., Nagle, J., Shiono, T., Ohura, T., Kominami, E. & Katunuma, N. (1986). Molecular cloning of human ornithine aminotransferase mRNA. Proceedings of the National Academy of Sciences of the United States of America 83, 1203-1207.
92. Itikawa, H., Baumberg, S. & Vogel, H. J. (1968). Enzymic basis for a genetic suppression: accumulation and deacylation of N-acetylglutamic γ-semialdehyde in enterobacterial mutants. Biochimica et Biophysica Acta - Bioenergetics 159, 547-550.
93. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2006). Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant and Cell Physiology 47, 141-153.
94. Ju, H. W., Min, J. H., Chung, M. S. & Kim, C. S. (2013). The atrzf1 mutation of the novel RING-type E3 ubiquitin ligase increases proline contents and enhances drought tolerance in Arabidopsis. Plant Science 203-204, 1-7.
95. Jung, Y., Park, J., Choi, Y., Yang, J. G., Kim, D., Kim, B. G., Roh, K., Lee, D. H., Auh, C. K. & Lee, S. (2010). Expression analysis of proline metabolism-related genes from halophyte Arabis stelleri under osmotic stress conditions. Journal of Integrative Plant Biology 52, 891-903.
96. Jung, C., Seo, J. S., Han, S. W., Koo, Y. J., Kim, C. H., Song, S. I., Nahm, B. H., Choi, Y. D. & Cheong, J. J. (2008). Overexpression of AtMYB44 enhances stomatal closure to confer abiotic stress tolerance in transgenic Arabidopsis. Plant Physiology 146, 623-635.
97. Kaino, T., Tasaka, Y., Tatehashi, Y. & Takagi, H. (2012). Functional analysis of the C-terminal region of γ-glutamyl kinase of Saccharomyces cerevisiae. Bioscience, Biotechnology, and Biochemistry 76, 454-461.
98. Kaplan-Levy, R. N., Brewer, P. B., Quon, T. & Smyth, D. R. (2012). The trihelix family of transcription factors - light, stress and development. Trends in Plant Science 17, 163-171.
99. Katchalsky, A. & Paecht, M. (1954). Phosphate anhydrides of amino acids. Journal of the American Chemical Society 76, 6042-6044.
100. Kemble, A. R. & Macpherson, H. T. (1954). Liberation of amino acids in perennial rye grass during wilting. Biochemical Journal 58, 46-49.
101. Kesari, R., Lasky, J. R., Villamor, J. G., Des Marais, D. L., Chen, Y. J. C., Liu, T. W., Lin, W., Juenger, T. E. & Verslues, P. E. (2012). Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation. Proceedings of the National Academy of Sciences of the United States of America 109, 9197-9202.
102. Kim, D. W., Shibato, J., Agrawal, G. K., Fujihara, S., Iwahashi, H., Kim du, H., Shim, I. & Rakwal, R. (2007). Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Molecules and Cells 24, 45-59.
103. 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology 108, 1387-1394.
104. Kishor, P. B. K., Sangam, S., Amrutha, R. N., Laxmi, P. S., Naidu, K. R., Rao, K. R. S. S., Rao, S., Reddy, K. J., 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. Current Science 88, 424-438.
105. Kizis, D., Lumbreras, V. & Pages, M. (2001). Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. The Federation of European Biochemical Societies Letters 498, 187-189.
106. Kosuge, T. & Hoshino, T. (1998). Construction of a proline-producing mutant of the extremely thermophilic eubacterium Thermus thermophilus HB27. Applied and Environmental Microbiology 64, 4328-4332.
107. Kumar, V., Shriram, V., Kavi Kishor, P. B., Jawali, N. & Shitole, M. G. (2010). Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over-expressing P5CSF129A gene. Plant Biotechnology Reports 4, 37-48.
108. Kuo, T.-T. & Stocker, B. A. D. (1969). Suppression of proline requirement of proA and proAB deletion mutants in Salmonella typhimurium by mutation to arginine requirement. Journal of Bacteriology 98, 593-598.
109. +-permeable conductance in root cells. Plant Cell 24, 1522-1533.
110. Lee, S. Y., Cho, J. Y., Lee, H. J., Kim, Y. H. & Min, J. (2010). Enhancement of ornithine production in proline-supplemented Corynebacterium glutamicum by ornithine cyclodeaminase. Journal of Microbiology and Biotechnology 20, 127-131.
111. Lee, J., He, K., Stolc, V., Lee, H., Figueroa, P., Gao, Y., Tongprasit, W., Zhao, H., Lee, I. & Deng, X. W. (2007). Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19, 731-749.
112. Lehmann, S., Funck, D., Szabados, L. & Rentsch, D. (2010). Proline metabolism and transport in plant development. Amino Acids 39, 949-962.
113. Leung, J., Bouvier-Durand, M., Morris, P. C., Guerrier, D., Chefdor, F. & Giraudat, J. (1994). Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448-1452.
114. Li, W. & Brandriss, M. C. (1992). Proline biosynthesis in Saccharomyces cerevisiae: molecular analysis of the PRO1 gene, which encodes γ-glutamyl kinase. Journal of Bacteriology 174, 4148-4156.
115. Li, Z. G., Ding, X. J. & Du, P. F. (2013). Hydrogen sulfide donor sodium hydrosulfide-improved heat tolerance in maize and involvement of proline. Journal of Plant Physiology 170, 741-747.
116. Li, B. & Simon, M. C. (2013). Molecular pathways: targeting MYC-induced metabolic reprogramming and oncogenic stress in cancer. Clinical Cancer Research 19, 5835-5841.
117. Limauro, D., Falciatore, A., Basso, A. L., Forlani, G. & De Felice, M. (1996). Proline biosynthesis in Streptococcus thermophilus: characterization of the proBA operon and its products. Microbiology 142, 3275-3282.
118. Liu, Y., Borchert, G. L., Donald, S. P., Diwan, B. A., Anver, M. & Phang, J. M. (2009). Proline oxidase functions as a mitochondrial tumor suppressor in human cancers. Cancer Research 69, 6414-6422.
119. Liu, Y., Borchert, G. L., Surazynski, A., Hu, C. A. & Phang, J. M. (2006). Proline oxidase activates both intrinsic and extrinsic pathways for apoptosis: the role of ROS/superoxides, NFAT and MEK/ERK signaling. Oncogene 25, 5640-5647.
120. Liu, Y., Borchert, G. L., Surazynski, A. & Phang, J. M. (2008). Proline oxidase, a p53-induced gene, targets COX-2/PGE2 signaling to induce apoptosis and inhibit tumor growth in colorectal cancers. Oncogene 27, 6729-6737.
121. Liu, R. J., Chen, T. & Cao, J. W. (2005). Construction of fused osmoregulation proBA gene from a salt-tolerant mutant of Bacillus subtilis and its influence on the osmotolerance of Escherichia coli. Acta Microbiologica Sinica 45, 23-26.
122. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391-1406.
123. Liu, W., Le, A., Hancock, C., Lane, A. N., Dang, C. V., Fan, T. W. & Phang, J. M. (2012). Reprogramming of proline and glutamine metabolism contributes to the proliferative and metabolic responses regulated by oncogenic transcription factor c-MYC. Proceedings of the National Academy of Sciences of the United States of America 109, 8983-8988.
124. Maggio, A., Miyazaki, S., Veronese, P., Fujita, T., Ibeas, J. I., Damsz, B., Narasimhan, M. L., Hasegawa, P. M., Joly, R. J. & Bressan, R. A. (2002). Does proline accumulation play an active role in stress-induced growth reduction? The Plant Journal 31, 699-712.
125. 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 Physiology 128, 73-83.
126. Marco-Marín, C., Gil-Ortiz, F., Pérez-Arellano, I., Cervera, J., Fita, I. & Rubio, V. (2007). A novel two-domain architecture within the amino acid kinase enzyme family revealed by the crystal structure of Escherichia coli glutamate 5-kinase. Journal of Molecular Biology 367, 1431-1446.
127. Martin, W., Rujan, T., Richly, E., Hansen, A., Cornelsen, S., Lins, T., Leister, D., Stoebe, B., Hasegawa, M. & Penny, D. (2002). Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proceedings of the National Academy of Sciences of the United States of America 99, 12246-12251.
128. Martinelli, D., Häberle, J., Rubio, V., Giunta, C., Hausser, I., Carrozzo, R., Gougeard, N., Marco-Marín, C., Goffredo, B., Meschini, M., Bevivino, E., Boenzi, S., Colafati, G., Brancati, F., Baumgartner, M. & Dionisi-Vici, C. (2012). Understanding pyrroline-5-carboxylate synthetase deficiency: clinical, molecular, functional, and expression studies, structure-based analysis, and novel therapy with arginine. Journal of Inherited Metabolic Disease 35, 761-776.
129. Massarelli, I., Forlani, G., Ricca, E. & De Felice, M. (2000). Enhanced and feedback-resistant γ-glutamyl kinase activity of an Escherichia coli transformant carrying a mutated proB gene of Streptococcus thermophilus. Federation of European Microbiological Societies Microbiology Letters 182, 143-147.
130. 1-pyrroline-5-carboxylate reductase from baker's yeast: further purification by affinity chromatography with 5′ AMP-sepharose 4B. Biochimica et Biophysica Acta 616, 381-383.
131. Mattioli, R., Falasca, G., Sabatini, S., Altamura, M. M., Costantino, P. & Trovato, M. (2009). The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiologia Plantarum 137, 72-85.
132. Mattioli, R., Marchese, D., D'Angeli, S., Altamura, M., Costantino, P. & Trovato, M. (2008). Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Molecular Biology 66, 277-288.
133. Mauro, M. L., Trovato, M., Paolis, A. D., Gallelli, A., Costantino, P. & Altamura, M. M. (1996). The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Developmental Biology 180, 693-700.
134. Maxwell, S. A. & Rivera, A. (2003). Proline oxidase induces apoptosis in tumor cells, and its expression is frequently absent or reduced in renal carcinomas. The Journal of Biological Chemistry 278, 9784-9789.
135. Meijer, P. J., Lilius, G., Holmberg, N. & Bülow, L. (1996). An artificial bifunctional enzyme, γ-glutamyl kinase/γ-glutamyl phosphate reductase, improves NaCl tolerance when expressed in Escherichia coli. Biotechnology Letters 18, 1133-1138.
136. Meng, Z., Lou, Z., Liu, Z., Li, M., Zhao, X., Bartlam, M. & Rao, Z. (2006). Crystal structure of human pyrroline-5-carboxylate reductase. Journal of Molecular Biology 359, 1364-1377.
137. Miao, L. X., Cao, J. W., Liu, R. J., Wang, Y. L. & Zeng, Y. H. (2002). Cloning and sequencing of the proBA gene from the selected mutant resistant to proline analogue from Bacillus subtilis. Acta Genetica Sinica 29, 1111-1117.
138. 1-pyrroline-5-carboxylate-proline cycle in plants by uncoupled expression of proline oxidation enzymes. Journal of Biological Chemistry 284, 26482-26492.
139. Milner, J. L., McClellan, D. J. & Wood, J. M. (1987). Factors reducing and promoting the effectiveness of proline as an osmoprotectant in Escherichia coli K12. Journal of General Microbiology 133, 1851-1860.
140. Morita, Y., Nakamori, S. & Takagi, H. (2003). L-proline accumulation and freeze tolerance in Saccharomyces cerevisiae are caused by a mutation in the PRO1 gene encoding γ-glutamyl kinase. Applied and Environmental Microbiology 69, 212-219.
141. 1-pyrroline-5-carboxylate reductase isoenzymes, indicating differential distribution in spinach (Spinacia oleracea L.) leaves. Plant and Cell Physiology 42, 742-750.
142. Muth, W. L. & Costilow, R. N. (1974a). Ornithine cyclase (deaminating): II. Properties of the homogeneous enzyme. Journal of Biological Chemistry 249, 7457-7462.
143. Muth, W. L. & Costilow, R. N. (1974b). Ornithine cyclase (deaminating): III. Mechanism of the conversion of ornithine to proline. Journal of Biological Chemistry 249, 7463-7467.
144. Nakamura, Y., Kaneko, T., Sato, S., Mimuro, M., Miyashita, H., Tsuchiya, T., Sasamoto, S., Watanabe, A., Kawashima, K., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Nakazaki, N., Shimpo, S., Takeuchi, C., Yamada, M. & Tabata, S. (2003). Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Research 10, 137-145.
145. Nanjo, T., Kobayashi, M., Yoshiba, Y., Kakubari, Y., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1999). Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. The Federation of European Biochemical Societies Letters 461, 205-210.
146. 1-pyrroline-5-carboxylate reductase from human pathogens Neisseria meningitides [sic] and Streptococcus pyogenes. Journal of Molecular Biology 354, 91-106.
147. 1-pyrroline-5-carboxylate reductase from tobacco leaves. Agricultural and Biological Chemistry 30, 452-456.
148. Omori, K., Suzuki, S. I., Imai, Y. & Komatsubara, S. (1991). Analysis of the Serratia marcescens proBA operon and feedback control of proline biosynthesis. Journal of General Microbiology 137, 509-517.
149. Omori, K., Suzuki, S. I., Imai, Y. & Komatsubara, S. (1992). Analysis of the mutant proBA operon from a proline-producing strain of Serratia marcescens. Journal of General Microbiology 138, 693-699.
150. Orser, C., Goodner, B., Johnston, M., Gelvin, S. & Csonka, L. (1988). The Escherichia coli proB gene corrects the proline auxotrophy of Saccharomyces cerevisiae pro1 mutants. Molecular and General Genetics MGG 212, 124-128.
151. Overbeek, R., Fonstein, M., D'Souza, M., Pusch, G. D. & Maltsev, N. (1999). The use of gene clusters to infer functional coupling. Proceedings of the National Academy of Sciences of the United States of America 96, 2896-2901.
152. Page, R., Nelson, M. S., von Delft, F., Elsliger, M.-A., Canaves, J. M., Brinen, L. S., Dai, X., Deacon, A. M., Floyd, R., Godzik, A., Grittini, C., Grzechnik, S. K., Jaroszewski, L., Klock, H. E., Koesema, E., Kovarik, J. S., Kreusch, A., Kuhn, P., Lesley, S. A., McMullan, D., McPhillips, T. M., Miller, M. D., Morse, A., Moy, K., Ouyang, J., Robb, A., Rodrigues, K., Schwarzenbacher, R., Spraggon, G., Stevens, R. C., van den Bedem, H., Velasquez, J., Vincent, J., Wang, X., West, B., Wolf, G., Hodgson, K. O., Wooley, J. & Wilson, I. A. (2004). Crystal structure of γ-glutamyl phosphate reductase (TM0293) from Thermotoga maritima at 2.0 Å resolution. Proteins: Structure, Function, and Bioinformatics 54, 157-161.
153. Papdi, C., Ábrahám, E., Joseph, M. P., Popescu, C., Koncz, C. & Szabados, L. (2008). Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiology 147, 528-542.
154. Parre, E., Ghars, M. A., Leprince, A.-S., 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 Physiology 144, 503-512.
155. 1-pyrroline-5-carboxylate synthetase activity. In Plant Stress Tolerance, Volume 639. Methods in Molecular Biology (ed. R. Sunkar ), pp. 333-340. Humana Press, New York.
156. Pérez-Arellano, I., Carmona-Álvarez, F., Gallego, J. & Cervera, J. (2010a). Molecular mechanisms modulating glutamate kinase activity. Identification of the proline feedback inhibitor binding site. Journal of Molecular Biology 404, 890-901.
157. Pérez-Arellano, I., Carmona-Álvarez, F., Martínez, A. I., Rodríguez-Díaz, J. & Cervera, J. (2010b). Pyrroline-5-carboxylate synthase and proline biosynthesis: from osmotolerance to rare metabolic disease. Protein Science 19, 372-382.
158. Pérez-Arellano, I., Gallego, J. & Cervera, J. (2007). The PUA domain - a structural and functional overview. The Federation of European Biochemical Societies Journal 274, 4972-4984.
159. Pérez-Arellano, I., Rubio, V. & Cervera, J. (2006). Mapping active site residues in glutamate-5-kinase. The substrate glutamate and the feed-back inhibitor proline bind at overlapping sites. The Federation of European Biochemical Societies Letters 580, 6247-6253.
160. Phang, J. M. & Liu, W. (2012). Proline metabolism and cancer. Frontiers in Bioscience 17, 1835-1845.
161. Phang, J. M., Liu, W., Hancock, C. & Christian, K. J. (2012). The proline regulatory axis and cancer. Frontiers in Oncology 2, 60, doi: 10.3389/fonc.2012.00060.
162. Phang, J. M., Liu, W. & Zabirnyk, O. (2010). Proline metabolism and microenvironmental stress. Annual Review of Nutrition 30, 441-463.
163. Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W. & Vogelstein, B. (1997). A model for p53-induced apoptosis. Nature 389, 300-305.
164. Possemato, R., Marks, K. M., Shaul, Y. D., Pacold, M. E., Kim, D., Birsoy, K., Sethumadhavan, S., Woo, H. K., Jang, H. G., Jha, A. K., Chen, W. W., Barrett, F. G., Stransky, N., Tsun, Z. Y., Cowley, G. S., Barretina, J., Kalaany, N. Y., Hsu, P. P., Ottina, K., Chan, A. M., Yuan, B., Garraway, L. A., Root, D. E., Mino-Kenudson, M., Brachtel, E. F., Driggers, E. M. & Sabatini, D. M. (2011). Functional genomics reveal that the serine synthesis pathway is essential in breast cancer. Nature 476, 346-350.
165. Rajaram, V., Ratna Prasuna, P., Savithri, H. S. & Murthy, M. R. (2008). Structure of biosynthetic N-acetylornithine aminotransferase from Salmonella typhimurium: studies on substrate specificity and inhibitor binding. Proteins 70, 429-441.
166. Rathinasabapathi, B. (2000). Progress and prospects in engineering crops for osmoprotectant synthesis. In Plant Tolerance to Abiotic Stresses in Agriculture: Role of Genetic Engineering (Volume 83), (eds J. H. Cherry, R. D. Locy, and A. Richter ) pp. 139-156. Kluwer Academic Publishers, Dordrecht, Netherlands.
167. Rayapati, P. J., Stewart, C. R. & Hack, E. (1989). Pyrroline-5-carboxylate reductase is in pea (Pisum sativum L.) leaf chloroplasts. Plant Physiology 91, 581-586.
168. Reversade, B., Escande-Beillard, N., Dimopoulou, A., Fischer, B., Chng, S. C., Li, Y., Shboul, M., Tham, P. Y., Kayserili, H., Al-Gazali, L., Shahwan, M., Brancati, F., Lee, H., O'Connor, B. D., Schmidt-von Kegler, M., Merriman, B., Nelson, S. F., Masri, A., Alkazaleh, F., Guerra, D., Ferrari, P., Nanda, A., Rajab, A., Markie, D., Gray, M., Nelson, J., Grix, A., Sommer, A., Savarirayan, R., Janecke, A. R., Steichen, E., Sillence, D., Hausser, I., Budde, B., Nurnberg, G., Nurnberg, P., Seemann, P., Kunkel, D., Zambruno, G., Dallapiccola, B., Schuelke, M., Robertson, S., Hamamy, H., Wollnik, B., Van Maldergem, L., Mundlos, S. & Kornak, U. (2009). Mutations in PYCR1 cause cutis laxa with progeroid features. Nature Genetics 41, 1016-1021.
169. Rhodes, D., Handa, S. & Bressan, R. A. (1986). Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiology 82, 890-903.
170. Richards, T. A., Dacks, J. B., Campbell, S. A., Blanchard, J. L., Foster, P. G., McLeod, R. & Roberts, C. W. (2006). Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryotic Cell 5, 1517-1531.
171. Riechmann, J. L. & Meyerowitz, E. M. (1998). The AP2/EREBP family of plant transcription factors. Biological Chemistry 379, 633-646.
172. Roosens, N. H., Thu, T. T., Iskandar, H. M. & Jacobs, M. (1998). Isolation of the ornithine-δ-aminotransferase cDNA and effect of salt stress on its expression in Arabidopsis thaliana. Plant Physiology 117, 263-271.
173. 1-pyrroline-5-carboxylate reductase from Escherichia coli. Journal of Bacteriology 129, 108-114.
174. Rushlow, K. E., Deutch, A. H. & Smith, C. J. (1985). Identification of a mutation that relieves gamma-glutamyl kinase from allosteric feedback inhibition by proline. Gene 39, 109-112.
175. Samach, A., Onouchi, H., Gold, S. E., Ditta, G. S., Schwarz-Sommer, Z., Yanofsky, M. F. & Coupland, G. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616.
176. Sangurdekar, D., Srienc, F. & Khodursky, A. (2006). A classification based framework for quantitative description of large-scale microarray data. Genome Biology 7, R32, doi: 10.1186/gb-2006-7-4-r32
177. Sans, N., Schröder, G. & Schröder, J. (1987). The Noc region of Ti plasmid C58 codes for arginase and ornithine cyclodeaminase. European Journal of Biochemistry 167, 81-87.
178. Saradhi, P. P., Alia, A. S. & Prasad, K. V. S. K. (1995). Proline accumulates in plants exposed to UV radiation and protects them against UV-induced peroxidation. Biochemical and Biophysical Research Communications 209, 1-5.
179. Sasano, Y., Haitani, Y., Ohtsu, I., Shima, J. & Takagi, H. (2012). Proline accumulation in baker's yeast enhances high-sucrose stress tolerance and fermentation ability in sweet dough. International Journal of Food Microbiology 152, 40-43.
180. Saum, S. H. & Müller, V. (2007). Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus. Journal of Bacteriology 189, 6968-6975.
181. Savouré, A., Hua, X. J., Bertauche, N., Montagu, M. V. & Verbruggen, N. (1997). Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Molecular and General Genetics MGG 254, 104-109.
182. Schat, H., Sharma, S. S. & Vooijs, R. (1997). Heavy metal-induced accumulation of free proline in a metal-tolerant and a nontolerant ecotype of Silene vulgaris. Physiologia Plantarum 101, 477-482.
183. Schroeter, R., Hoffmann, T., Voigt, B., Meyer, H., Bleisteiner, M., Muntel, J., Jörgen, B., Albrecht, D., Becher, D., Lalk, M., Evers, S., Bongaerts, J., Maurer, K. H., Putzer, H., Hecker, M., Schweder, T. & Bremer, E. (2013). Stress responses of the industrial workhorse Bacillus licheniformis to osmotic challenges. PLos One 8, e80956.
184. Schulz, T. J., Zarse, K., Voigt, A., Urban, N., Birringer, M. & Ristow, M. (2007). Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metabolism 6, 280-293.
185. Seddon, A. P., Zhao, K. Y. & Meister, A. (1989). Activation of glutamate by γ-glutamate kinase: formation of gamma-cis-cycloglutamyl phosphate, an analog of γ-glutamyl phosphate. Journal of Biological Chemistry 264, 11326-11335.
186. Sekine, T., Kawaguchi, A., Hamano, Y. & Takagi, H. (2007). Desensitization of feedback inhibition of the Saccharomyces cerevisiae γ-glutamyl kinase enhances proline accumulation and freezing tolerance. Applied and Environmental Microbiology 73, 4011-4019.
187. Senthil-Kumar, M. & Mysore, K. S. (2012). Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant, Cell & Environment 35, 1329-1343.
188. Serebrijski, I., Wojcik, F., Reyes, O. & Leblon, G. (1995). Multicopy suppression by asd gene and osmotic stress-dependent complementation by heterologous proA in proA mutants. Journal of Bacteriology 177, 7255-7260.
189. Servet, C., Ghelis, T., Richard, L., Zilberstein, A. & Savouré, A. (2012). Proline dehydrogenase: a key enzyme in controlling cellular homeostasis. Frontiers in Bioscience 17, 607-620.
190. Sharma, S. & Verslues, P. E. (2010). Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant, Cell & Environment 33, 1838-1851.
191. Shen, B. W., Hennig, M., Hohenester, E., Jansonius, J. N. & Schirmer, T. (1998). Crystal structure of human recombinant ornithine aminotransferase. Journal of Molecular Biology 277, 81-102.
192. Shinozaki, K. & Yamaguchi-Shinozaki, K. (2000). Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 3, 217-223.
193. Shultz, J. L., Kurunam, D., Shopinski, K., Iqbal, M. J., Kazi, S., Zobrist, K., Bashir, R., Yaegashi, S., Lavu, N., Afzal, A. J., Yesudas, C. R., Kassem, M. A., Wu, C., Zhang, H. B., Town, C. D., Meksem, K. & Lightfoot, D. A. (2006). The Soybean Genome Database (SoyGD): a browser for display of duplicated, polyploid, regions and sequence tagged sites on the integrated physical and genetic maps of Glycine max. Nucleic Acids Research 34, D758-D765.
194. Silva-Ortega, C. O., Ochoa-Alfaro, A. E., Reyes-Agüero, J. A., Aguado-Santacruz, G. A. & Jiménez-Bremont, J. F. (2008). Salt stress increases the expression of p5cs gene and induces proline accumulation in cactus pear. Plant Physiology and Biochemistry 46, 82-92.
195. Singh, V., Bhatt, I., Aggarwal, A., Tripathi, B., Munjal, A. & Sharma, V. (2010). Proline improves copper tolerance in chickpea (Cicer arietinum). Protoplasma 245, 173-181.
196. Siripornadulsil, S., Traina, S., Verma, D. P. S. & Sayre, R. T. (2002). Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell 14, 2837-2847.
197. Sleator, R. D., Gahan, C. G. M. & Hill, C. (2001). Mutations in the listerial proB gene leading to proline overproduction: effects on salt tolerance and murine infection. Applied and Environmental Microbiology 67, 4560-4565.
198. Smirnoff, N. & Cumbes, Q. J. (1989). Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057-1060.
199. Smith, C. J., Deutch, A. H. & Rushlow, K. E. (1984). Purification and characteristics of a γ-glutamyl kinase involved in Escherichia coli proline biosynthesis. Journal of Bacteriology 157, 545-551.
200. Song, S., Chen, Y., Zhao, M. & Zhang, W. H. (2012). A novel Medicago truncatula HD-Zip gene, MtHB2, is involved in abiotic stress responses. Environmental and Experimental Botany 80, 1-9.
201. Soto, M. J., Zorzano, A., Garcia-Rodriguez, F. M., Mercado-Blanco, J., Lopez-Lara, I. M., Olivares, J. & Toro, N. (1994). Identification of a novel Rhizobium meliloti nodulation efficiency nfe gene homolog of Agrobacterium ornithine cyclodeaminase. Molecular Plant-Microbe Interactions 7, 703-707.
202. Steil, L., Hoffmann, T., Budde, I., Völker, U. & Bremer, E. (2003). Genome-wide transcriptional profiling analysis of adaptation of Bacillus subtilis to high salinity. Journal of Bacteriology 185, 6358-6370.
203. Stein, H., Honig, A., Miller, G., Erster, O., Eilenberg, H., Csonka, L. N., Szabados, L., Koncz, C. & Zilberstein, A. (2011). Elevation of free proline and proline-rich protein levels by simultaneous manipulations of proline biosynthesis and degradation in plants. Plant Science 181, 140-150.
204. Stewart, C. R. & Voetberg, G. (1985). Relationship between stress-induced ABA and proline accumulations and ABA-induced proline accumulation in excised barley leaves. Plant Physiology 79, 24-27.
205. Stewart, C. R. & Voetberg, G. (1987). Abscisic acid accumulation is not required for proline accumulation in wilted leaves. Plant Physiology 83, 747-749.
206. 1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiology 120, 923.
207. Stránská, J., Kopečný, D., Tylichová, M., Snégaroff, J. & Šebela, M. (2008). Ornithine-δ-aminotransferase: an enzyme implicated in salt tolerance in higher plants. Plant Signaling & Behavior 3, 929-935.
208. Strizhov, N., Ábrahám, E., Ökrész, 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. The Plant Journal 12, 557-569.
209. Szabados, L., Kovács, H., Zilberstein, A. & Bouchereau, A. (2011). Plants in extreme environments: importance of protective compounds in stress tolerance. In Plant Responses to Drought and Salinity Stress Developments in a Post-Genomic Era, Advances in Botanical Research, Volume 57 (ed. I. Turkan ), pp. 105-150. Academic Press, Orlando.
210. Szabados, L. & Savouré, A. (2010). Proline: a multifunctional amino acid. Trends in Plant Science 15, 89-97.
211. Székely, G., Ábrahám, E., Cséplö, A., Rigó, G., Zsigmond, L., Csiszár, 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. The Plant Journal 53, 11-28.
212. 1-pyrroline-5-carboxylate reductase in root/nodule and leaf of soybean. Plant Physiology 99, 1642-1659
213. Tan, B. S., Lonic, A., Morris, M. B., Rathjen, P. D. & Rathjen, J. (2011). The amino acid transporter SNAT2 mediates L-proline-induced differentiation of ES cells. American Journal of Physiology - Cell Physiology 300, C1270-C1279.
214. Tempest, D. W., Meers, J. L. & Brown, C. M. (1970). Influence of environment on the content and composition of microbial free amino acid pools. Journal of General Microbiology 64, 171-185.
215. Terao, Y., Nakamori, S. & Takagi, H. (2003). Gene dosage effect of L-proline biosynthetic enzymes on L-proline accumulation and freeze tolerance in Saccharomyces cerevisiae. Applied and Environmental Microbiology 69, 6527-6532.
216. Toka, I., Planchais, S., Cabassa, C., Justin, A.-M., De Vos, D., Richard, L., Savouré, A. & Carol, P. (2010). Mutations in the hyperosmotic stress-responsive mitochondrial BASIC AMINO ACID CARRIER2 enhance proline accumulation in Arabidopsis. Plant Physiology 152, 1851-1862.
217. Tomenchok, D. M. & Brandriss, M. C. (1987). Gene-enzyme relationships in the proline biosynthetic pathway of Saccharomyces cerevisiae. Journal of Bacteriology 169, 5364-5372.
218. Tomlinson, C., Rafii, M., Ball, R. O. & Pencharz, P. B. (2011). Arginine can be synthesized from enteral proline in healthy adult humans. The Journal of Nutrition 141, 1432-1436.
219. Trovato, M., Maras, B., Linhares, F. & Costantino, P. (2001). The plant oncogene rolD encodes a functional ornithine cyclodeaminase. Proceedings of the National Academy of Sciences of the United States of America 98, 13449-13453.
220. Urao, T., Noji, M.-a., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1996). A transcriptional activation domain of ATMYB2, a drought-inducible Arabidopsis Myb-related protein. The Plant Journal 10, 1145-1148.
221. Veeravalli, K., Boyd, D., Iverson, B. L., Beckwith, J. & Georgiou, G. (2011). Laboratory evolution of glutathione biosynthesis reveals natural compensatory pathways. Nature Chemical Biology 7, 101-105.
222. Verbruggen, N., Villarroel, R. & Van Montagu, M. (1993). Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiology 103, 771-781.
223. Verslues, P., Kim, Y. S. & Zhu, J. K. (2007). Altered ABA, proline and hydrogen peroxide in an Arabidopsis glutamate: glyoxylate aminotransferase mutant. Plant Molecular Biology 64, 205-217.
224. Verslues, P. E. & Sharma, S. (2010). Proline metabolism and its implications for plant-environment interaction. In The Arabidopsis Book, e0140. doi: 10.1199/tab.0140. The American Society of Plant Biologists, Rockville MD.
225. Voetberg, G. & Stewart, C. R. (1984). Steady state proline levels in salt-shocked barley leaves. Plant Physiology 76, 567-570.
226. Von Blohn, C., Kempf, B., Kappes, R. M. & Bremer, E. (1997). Osmostress response in Bacillus subtilis: characterization of a proline uptake system (OpuE) regulated by high osmolarity and the alternative transcription factor sigma B. Molecular Microbiology 25, 175-187.
227. Wächter, R., Langhans, M., Aloni, R., Götz, S., Weilmünster, A., Koops, A., Temguia, L., Mistrik, I., Pavlovkin, J., Rascher, U., Schwalm, K., Koch, K. E. & Ullrich, C. I. (2003). Vascularization, high-volume solution flow, and localized roles for enzymes of sucrose metabolism during tumorigenesis by Agrobacterium tumefaciens. Plant Physiology 133, 1024-1037.
228. Washington, J. M., Rathjen, J., Felquer, F., Lonic, A., Bettess, M. D., Hamra, N., Semendric, L., Tan, B. S., Lake, J. A., Keough, R. A., Morris, M. B. & Rathjen, P. D. (2010). L-proline induces differentiation of ES cells: a novel role for an amino acid in the regulation of pluripotent cells in culture. American Journal of Physiology - Cell Physiology 298, C982-C992.
229. Xin, Z. & Browse, J. (1998). eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant. Proceedings of the National Academy of Sciences of the United States of America 95, 7799-7804.
230. Xin, Z., Mandaokar, A., Chen, J., Last, R. L. & Browse, J. (2007). Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. The Plant Journal 49, 786-799.
231. Xue, Y., Peng, R., Xiong, A., Li, X., Zha, D. & Yao, Q. (2009). Yeast heat-shock protein gene HSP26 enhances freezing tolerance in Arabidopsis. Journal of Plant Physiology 166, 844-850.
232. Yang, S. L., Lan, S. S. & Gong, M. (2009). Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. Journal of Plant Physiology 166, 1694-1699.
233. Yoo, J. H., Park, C. Y., Kim, J. C., Do Heo, W., Cheong, M. S., Park, H. C., Kim, M. C., Moon, B. C., Choi, M. S., Kang, Y. H., Lee, J. H., Kim, H. S., Lee, S. M., Yoon, H. W., Lim, C. O., Yun, D.-J., Lee, S. Y., Chung, W. S. & Cho, M. J. (2005). Direct interaction of a divergent CaM isoform and the transcription factor, MYB2, enhances salt tolerance in Arabidopsis. Journal of Biological Chemistry 280, 3697-3706.
234. 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. The Plant Journal 7, 751-760.
235. 1-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochemical and Biophysical Research Communications 261, 766-772.
236. Zaprasis, A., Hoffmann, T., Wunsche, G., Florez, L. A., Stulke, J. & Bremer, E. (2014). Mutational activation of the rocR activator and of a cryptic rocDEF promoter bypass loss of the initial steps of proline biosynthesis in Bacillus subtilis. Environmental Microbiology 16, 701-717.
237. Zarse, K., Schmeisser, S., Groth, M., Priebe, S., Beuster, G., Kuhlow, D., Guthke, R., Platzer, M., Kahn, C. R. & Ristow, M. (2012). Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal. Cell Metabolism 15, 451-465.
238. Zhang, Z., Li, F., Li, D., Zhang, H. & Huang, R. (2010). Expression of ethylene response factor JERF1 in rice improves tolerance to drought. Planta 232, 765-774.
239. 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. Journal of Biological Chemistry 270, 20491-20496.
240. 1-pyrroline-5-carboxylate synthetase gene promoter in transgenic Arabidopsis thaliana subjected to water stress. Plant Science 129, 81-89.
241. Zhao, M. G., Chen, L., Zhang, L. L. & Zhang, W. H. (2009). Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiology 151, 755-767.
242. Zhou, G. A., Chang, R. Z. & Qiu, L. J. (2010). Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Molecular Biology 72, 357-367.
243. Zhu, Y., Shearer, G. & Kohl, D. H. (1992). Proline fed to intact soybean plants influences acetylene reducing activity and content and metabolism of proline in bacteroids. Plant Physiology 98, 1020-1028.
244. Zhu, Q., Zhang, J. T., Gao, X. S., Tong, J. H., Xiao, L. T., Li, W. B. & Zhang, H. X. (2010). The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457, 1-12.