Does proline accumulation play an active role in stress-induced growth reduction?

Plant Journal

Volumn 31, Issue 6, 2002, Pages 699-712

  Maggio, Albino ^a,c   Miyazaki, Saori ^a,d   Veronese, Paola ^a   Fujita, Tomomichi ^b,e   Ibeas, José I ^a,f   Damsz, Barbara ^a   Narasimhan, Meena L ^a   Hasegawa, Paul M ^a   Joly, Robert J ^a   Bressan, Ray A ^a  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c National Center of Energy   (Italy)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^f UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Microarray; Osmolytes; Ploidy; Signal transduction; Vacuolation

Indexed keywords

CELLS; DERIVATIVES; ENZYMES; SIGNALING; STRESSES;

OSMOLYTES; TRANSGENIC PLANTS; VACUOLATION;

PLANTS (BOTANY);

1-PYRROLINE-5-CARBOXYLATE DEHYDROGENASE; AMINO ACID SUBSTITUTION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LYCOPERSICON ESCULENTUM; MODELS, BIOLOGICAL; MUTATION; ORGANISMS, GENETICALLY MODIFIED; OSMOTIC PRESSURE; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PROLINE; PROLINE OXIDASE; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, PROTEIN; SIGNAL TRANSDUCTION; SODIUM CHLORIDE;

LYCOPERSICON ESCULENTUM; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 18544387781     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01389.x     Document Type: Article

References (61)

1. Aspinall, D. and Paleg, L.G. (1981) Proline accumulation: physiological aspects. In Physiology and Biochemistry of Drought Resistance in Plants (Paleg, L.G. and Aspinall, D., eds). Sidney, Australia: Academic Press, pp. 205-241.
2. Baluska, F. and Kubica, S. (1992) Relationships between the content of basic nuclear proteins, chromatin structure, rDNA transcription and cell size in different tissues of the maize root apex. J. Exp. Bot. 43, 991-996.
3. Bennett, M.D. and Smith, J.B. (1976) Nuclear DNA amounts in angiosperms. Phil. Trans. R. Soc. Lond. B, Biol. Sci. 274, 227-274.
4. Blomberg, A. and Adler, L. (1992) Physiology of osmotolerance in fungi. In Advances in Microbial Physiology, Vol. 33 (Rose, A.H., ed.). San Diego, CA: Academic Press, pp. 145-212.
5. Blum, A., Munns, R., Passioura, J.B. and Turner, N.C. (1996) Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations? Plant Physiol. 110, 1051-1053.
6. Bohnert, H.J. and Shen, B. (1999) Transformation and compatible solutes. Sci. Hortic. 78, 237-260.
7. Bone, N., Millar, J.B.A., Toda, T. and Armstrong, J. (1998) Regulated vacuole fusion and fission in Schizosaccharomyces pombe: an osmotic response dependent on MAP kinases. Curr. Biol. 8, 135-144.
8. Brandriss, M.C. (1979) Isolation and preliminary characterization of Saccharomyces cerevisiae proline auxotrophs. J. Bacteriol. 138, 816-822.
9. Bressan, R.A., Nelson, D.E., Iraki, N.M., LaRosa, P.C., Singh, N.K., Hasegawa, P.M. and Carpita, N.C. (1990) Reduced cell expansion and changes in cell walls of plant cells adapted to NaCl. In Environmental Injury to Plants (Katterman, F., ed.). San Diego, CA: Academic Press, pp. 137-171.
10. Chang, P.F.L., Damsz, B., Kononowicz, A.K. et al. (1996) Alterations in cell membrane structure and expression of a membrane-associated protein after adaptation to osmotic stress. Physiol. Plant. 98, 505-516.
11. Cohen, G.N. and Rickenberg, H.V. (1956) Concentration specifique reversible des amino acids chez E. coll. Ann. Inst Pasteur (Paris), 91, 693-720.
12. Csonka, L.N. (1981) Proline overproduction results in enhanced osmotolerance in Salmonella typhimurium. Mol. Gen. Genet. 182, 82-86.
13. Csonka, L.N. and Baich, A. (1983) Proline biosynthesis. In Amino Acids Biosynthesis and Genetic Regulation (Herrmann, K.M. and Somerville, R.L., eds). Reading, MA: Addison-Wesley Co., pp. 35-51.
14. Csonka, LN., Gelvin, S.B., Goodner, B.W., Orser, C.S., Siemieniak, D. and Slightom, J.L. (1988) Nucleotide sequence of a mutation in the proB gene in Escherichia coli that confers proline overproduction and enhanced tolerance of osmotic stress. Gene, 64, 199-205.
15. De Rocher, E.J., Harkins, K.R., Galbraith, D.W. and Bohnert, H.J. (1990) Developmentally regulated systemic endopolyploidy in sucullents with small genomes. Science, 250, 99-101.
16. Delauney, A.J., Hu, C.-A.A., Kavi Kishor, P.B. and Verma, D.P.S. (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.
17. Frommer, W.B., Ludewig, U. and Rentsch, D. (1999) Taking transgenic plants with a pinch of salt. Science, 285, 1222-1223.
18. 1-pyrroline-5-carboxylate synthetase from tomato. Plant Physiol. 118, 661-674.
19. Galitski, T., Saldanha, A.J., Styles, C.A., Lander, E.S. and Fink, G.R. (1999) Ploidy regulation of gene expression. Science, 285, 251-254.
20. Garcia, A.B., Engler, J.D.A., Iyer, S., Gerats, T., Van Montagu, M. and Caplan, A.B. (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol. 115, 159-169.
21. Grafi, G. and Larkins, B.A. (1995) Endoreduplication in maize endosperm: involvement of M phase-promoting factor inhibition and induction of S phase-related kinases. Science, 269, 1262-1264.
22. Grant, M.M., Brown, A.S., Corwin, L.M., Troxler, R.F. and Franzblau, C. (1975) Effects of 1-azetidine 2-carboxylic acid on growth and proline metabolism in Escherichia coli. Biochim. Biophys. Acta, 404, 180-187.
23. Gustin, M.C., Albertyn, J., Alexander, M. and Davenport, K. (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 62, 1264-1300.
24. Guthrie, C. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. San Diego, CA: Academic Press.
25. Handa, S., Handa, A.K., Hasegawa, P.M. and Bressan, R.A. (1986) Proline accumulation and the adaptation of cultured plant cells to water stress. Plant Physiol. 80, 938-945.
26. Hardwick, J.S., Kuruvilla, F.G., Tong, J.K., Shamji, A.F. and Schreiber, S.L (1999) Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc. Natl Acad. Sci. USA, 96, 14866-14870.
27. Hare, P.D. and Cress, W.A. (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul. 21, 79-102.
28. Hasegawa, P.M., Bressan, R.A., Zhu, J.-K. and Bohnert, H.J. (2000) Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463-499.
29. Hayashi, H., Alia, Mustardy, L., Deshnium, P., Ida, M. and Murata, N. (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase: accumulation of glycinbetaine and enhanced tolerance to salt and cold stress. Plant J. 12, 133-142.
30. Hellmann, H., Funck, D., Rentsch, D. and Frommer, W.B. (2000) Hypersensitivity of an Arabidopsis sugar signaling mutant toward exogenous proline application. Plant Physiol. 123, 779-790.
31. Holmström, K.-O., Mäntylä, E., Welin, B., Mandal, A., Tapio Palva, E., Tunnela, O.E. and Londesborough, J. (1996) Drought tolerance in tobacco. Nature, 379, 683-684.
32. 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol. 122, 1129-1136.
33. 1-pyrroline-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc. Natl Acad. Sci. USA, 89, 9354-9358.
34. Joly, R.J. and Hahn, D.T. (1989) An empirical model for leaf expansion in cacao in relation to plant water deficit. Ann. Bot. 64, 1-8.
35. Karakas, B., Ozias-Akins, P., Stushnoff, C., Suefferheld, M. and Rieger, M. (1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant, Cell Environ. 20, 609-616.
36. 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108, 1387-1394.
37. Kawasaki, S., Borchert, C., Deyholos, M., Wang, H., Brazille, S., Kawai, K., Galbraith, D.W. and Bohnert, H.J. (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell, 13, 889-905.
38. Kononowicz, A.K., Hasegawa, P.M. and Bressan, R.A. (1990) Chromosome number and nuclear DNA content of plants regenerated from salt adapted plant cells. Plant Cell Rep. 8, 676-679.
39. Liu, J. and Zhu, J.-K. (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol. 114, 591-596.
40. Maggio, A., Garcia-Rios, M., Fujita, T., Bressan, R.A., Joly, R.J., Hasegawa, P.M. and Csonka, L.N. (1996) Cloning of tomPRO1 (accession, U27454) and tomPRO2 (accession, U60267) from Lycopersicon esculentum L. Coexistence of polycistronic and monocistronic genes which encode the enzymes catalyzing the first two steps of proline biosynthesis. Plant Physiol. 112, 862(PGR 96-077).
41. Maggio, A., Bressan, R.A., Hasegawa, P.M. and Locy, R.D. (1997) Moderately increased constitutive proline does not alter osmotic stress tolerance. Physiol. Plant. 101, 240-246.
42. Morgan, J.M. (1984) Osmoregulation and water stress in higher plants. Annu. Rev. Plant Physiol. 35, 299-319.
43. Orser, C.S., Goodner, B.W., Johnston, M., Gelvin, S.B. and Csonka, L.N. (1988) The Escherichia coli proB gene corrects the proline auxotrophy of Saccharomyces cerevisiae pro1 mutants. Mol. Gen. Genet. 212, 124-128.
44. Pilon-Smits, E.A.H., Ebskamp, M.J.M., Paul, M.J., Jeuken, M.J.W., Weisbeek, P.J. and Smeekens, S.C.M. (1995) Improved performance of transgenic fructan-accumulating tobacco under water stress. Plant Physiol. 107, 125-130.
45. Rhodes, D. and Samaras, Y. (1994) Genetic control of osmoregulation in plants. In Cellular and Molecular Physiology of Cell Volume Regulation (Strange, K., ed.). Boca Raton, FL; CRC Press, pp. 347-361.
46. Romero, C., Belles, J.M., Vaya, J.L., Serrano, R. and Cullánez-Macia, F.A. (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta, 201, 293-297.
47. Samaras, Y., Bressan, R.A., Csonka, L.N., Garcia-Rios, M.G., Paino D'Urzo, M. and Rhodes, D. (1995) Proline accumulation during drought and salinity. In Environment and Plant Metabolism (Smirnoff, N., ed.). Oxford, UK: Bios Scientific Publishers Ltd, pp. 161-187.
48. Sharp, R.E., Boyer, J.S., Nguyen, H.T. and Hsiao, T.C. (1996) Genetically engineered plants resistant to soil drying and salt stress: how to interpret osmotic relations? Plant Physiol. 110, 1051-1053.
49. Sheveleva, E., Chmara, W., Bohnert, H.J. and Jensen, R.G. (1997) Increased salt and drought tolerance by D-Ononitol production in transgenic Nicotiana tabacum L. Plant Physiol. 115, 1211-1219.
50. Shinozaki, K. and Yamaguchi-Shinozaki, K. (1996) Molecular responses to drought and cold stress. Curr. Opin. Biotechnol. 7, 161-167.
51. Tarczynski, M.C., Jensen, R.G. and Bohnert, H.J. (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science, 259, 508-510.
52. Thompson, J.F. (1980) Arginine synthesis, proline synthesis, and related processes. In The Biochemistry of Plants, Vol. 5 (Miflin, B.J., ed,). New York, NY: Academic Press, pp. 375-402.
53. Troll, W. and Lindsley, J. (1955) A photometric method for the determination of proline. J. Biol. Chem. 215, 655-660.
54. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T. and Shinozaki, K. (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor, Plant Cell, 11, 1743-1754.
55. Voetberg, G.S. and Sharp, R.E. (1991) Growth of the maize primary root at Iow water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol. 96, 1125-1130.
56. Wang, S.-S. and Brandriss, M.C. (1986) Proline utilization in Saccharomyces cerevisiae: analysis of the cloned PUT1 gene. Mol. Cell. Biol. 6, 2638-2645.
57. Werner, J.E. and Finkelstein, R.R. (1995) Arabidopsis mutants with reduced response to NaCl and osmotic stress. Physiol. Plant. 93, 659-666.
58. Wu, S.-J., Ding, L. and Zhu, J.-K. (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell, 8, 617-627.
59. Yancey, P.H. (1994) Compatible and counteracting solutes. In Cellular and Molecular Physiology of Cell Volume Regulation (Strange, K., ed.), Boca Raton, FL: CRC Press, pp. 81-109.
60. Yun, D.J., Ibeas, J.I., Lee, H., Coca, M.A., Narasimhan, M.L., Uesono, Y., Hasegawa, P.M., Pardo, J.M. and Bressan, R.A. (1998) Osmotin, a plant antifungal protein, subverts signal transduction to enhance fungal cell susceptibility. Mol. Cell, 1, 807-817.
61. 1-pyrroline-5-carboxylate synthetase, a bifunctional enzyme catalyzing the first two steps of proline biosynthesis in plants. J. Biol. Chem. 270, 20491-20496.