Abstract
Monocotyledonous leaves subjected to osmotica used for protoplast isolation accumulate a massive amount of putrescine (Put), lose chlorophyll and senesce rapidly. Treatment with spermidine (Spd) or spermine (Spm) prevents the loss of chlorophyll, indicating preservation of the thylakoid membranes at the site of the chlorophyll-protein complexes. Using several recently produced antibody probes, the effects on the stabilization of thylakoid membranes of applying either difluoromethylarginine (DFMA), a specific inhibitor of putrescine synthesis via arginine decarboxylase, or the polyamines Spd, Spm, or diaminopropane (Dap) to osmotically shocked oat leaves (Avena sativa L.) have been investigated. High protein levels were maintained in thylakoid membranes of leaf tissue incubated in the dark in the presence of 0.6 M sorbitol when pretreated with DFMA. After 48 h incubation, the level of the thylakoid protein D1, at the core of photosystem II, was higher in the DFMA-pretreated leaves as was the stromal protein ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco; as indicated by the level of large subunits). Applications of Spd, Spm or Dap were effective in retarding the loss of D1, D2 and cytochrome f from the thylakoid membranes as well as Rubisco large subunits and chlorophyll from the leaf tissue. The effects of polyamine applications may be mediated through Dap since most of the added Spd or Spm was converted to Dap within 6 h. The possible mechanisms of action of polyamine applications and DFMA-pretreatment on stabilizing the composition of the thylakoid membrane are also discussed.
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Abbreviations
- Cyt:
-
cytochrome
- Dap:
-
diaminopropane
- DFMA:
-
DL-α-difluoromethylarginine
- LSU:
-
large subunit (of Rubisco)
- Put:
-
putrescine
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase-oxygenase
- Spd:
-
spermidine
- Spm:
-
spermine
- SDS-PAGE:
-
sodium dodecyl sulphate-polyacrylamide gel electrophoresis
References
Altman, A. (1982) Retardation of radish leaf senescence by polyamines. Physiol. Plant. 54, 189–193
Altman, A., Kaur-Sawhney, R., Galston, A.W. (1977) Stabilization of oat protoplasts through polyamine-mediated inhibition of senescence. Plant Physiol. 60, 570–574
Arnon, D. (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol. 24, 1–15
Bagni, N., Serafini-Fracassini, D. (1973) The role of polyamines as growth factors in higher plants and their mechanism of action. In: Plant growth substances, pp. 1205–1217, Hirokawa Publ. Co., Tokyo
Barber, J. (1982) Influence of surface charges on thylakoid structure and function. Annu. Rev. Plant Physiol. 33, 261–295
Ben-David, H., Nelson, N., Gepstein, S. (1983) Differential changes in the amount of protein complexes in the chloroplast membrane during senescence of oat and bean leaves. Plant Physiol. 73, 507–510
Besford, R.T. (1989) Site-directed antibodies to the core proteins of photosystem 2. In: Institute of Horticultural Research, Annual Report 1989, pp. 38–39
Besford, R.T. (1990) The greenhouse effect: acclimation of tomato plants growing in high CO2, relative changes in Calvin cycle enzymes. J. Plant Physiol. 136, 458–463
Besford, R.T., Thomas, B. (1988) Production of monoclonal antibodies to thylakoid proteins. In: Environmental constraints on photosynthesis and the potential for genetic engineering, p. 50, Barber, J. ed. Agricultural and Food Research Council, London
Besford, R.T., Thomas, B., Huskisson, N.S., Butcher, G.W. (1990) Characterization of conformers of D1 of photosystem II using site-directed antibodies. Z. Naturforsch. 45c, 621–626
Capell, T., Campos, J.L., Tiburcio, A.F. (1992) Antisenescence properties of guazatine in osmotically-stressed oat leaves. Phytochemistry, in press
Cohen, A.S., Popovic, R.B., Zalik, S. (1979) Effects of polyamines on chlorophyll and protein content, photochemical activity, and chloroplast ultrastructure of barley leaf discs during senescence. Plant Physiol. 64, 717–780
Cohen, A.S., Balint, R., Sindhu, R.K. (1981) The synthesis of polyamines from methionine in intact and disrupted leaf protoplasts of virus-infected Chinese cabbage. Plant Physiol. 68, 1150–1155
Drolet, G., Dumbroff, E.B., Legge, R.L., Thompson, J.E. (1986) Radical scavenging properties of polyamines. Phytochemistry 25, 367–371
Flores, H.E., Galston, A.W. (1984) Osmotic stress-induced polyamine accumulation in cereal leaves. Plant Physiol. 75, 102–109
Fuhrer, J., Kaur-Sawhney, R., Shih, L.M., Galston, A.W. (1982) Effects of exogenous 1,3-diaminopropane and spermidine on senescence of oat leaves. Plant Physiol. 70, 1597–1600
Galston, A.W., Altman, A., Kaur-Sawhney, R. (1978) Polyamines, ribonuclease and the improvement of oat leaf protoplasts. Plant Sci. Lett. 11, 69–79
Harwood, J.L., Jones, A.V.H.M., Thomas, H. (1982) Leaf senescence in a nonyellowing mutant of Festuca pratensis. Planta 156, 152–157
Holloway, P.J., Maclean, D.J., Scott, K.J. (1983) Rate-limiting steps of electron transport in chloroplasts during ontogeny and senescence of barley. Plant Physiol. 72, 795–801
Kaur-Sawhney, R., Galston, A.W. (1979) Interaction of polyamines and light on biochemical processes involved in leaf senescence. Plant Cell Environ. 2, 189–196
Kaur-Sawhney, R., Flores, H.E., Galston, A.W. (1980) Polyamine-induced DNA synthesis and mitosis in oat leaf protoplasts. Plant Physiol. 65, 368–371
Li, N., Parsons, B.L., Liu, D., Mattoo, A.K. (1992) Accumulation of wound-inducible ACC synthase transcript in tomato fruit is inhibited by a slicylic acid and polyamines. Plant Mol. Biol. 18, 477–487
MacKinney, G. (1941) Absorption of light by chlorophyll solution. J. Biol. Chem. 140, 315–322
Popovic, R.B., Kyle, D.J., Cohen, A.S., Zalik, S. (1979) Stabilization of thylakoid membranes by spermine during stress-induced senescence of barley leaf discs. Plant Physiol. 64, 721–726
Roberts, D.R., Dumbroff, E.B., Thompson, J.E. (1986) Exogenous polyamines alter membrane fluidity in bean leaves — a basis for potential misinterpretation of their true physiological role. Planta 167, 395–401
Sechi, A.M., Cabrini, L., Laudi, L., Pasquali, P., Lenaz, G. (1978) Inhibition of phospholipase A2 and phospholipase C by polyamines. Arch. Biochem. Biophys. 186, 248–254
Sindhu, R.K., Cohen, S.S. (1984) Subcellular localization of spermidine synthase in the protoplast of Chinese cabbage leaves. Plant Physiol. 76, 219–223
Slocum, R.D., Kaur-Sawhney, R., Galston, A.W. (1984) The physiology and biochemistry of polyamines in higher plants. Arch. Biochem. Biophys. 235, 283–303
Smith, T.A. (1985) The inhibition and activation of polyamine oxidase from oat seedlings. Plant Growth Regul. 3, 269–275
Srivastava, S.K., Smith, T.A. (1981) The effect of some oligoamines and guanidines on membrane permeability in higher plants. Phytochemistry 21, 997–1008
Takabe, T., Takabe, T., Akazawa, T. (1986) Biosynthesis of P700-chlorophyll a protein complex, plastocyanin, and cytochrome b6f complex. Plant Physiol. 81, 60–66
Tiburcio, A.F., Kaur-Sawhney, R., Galston, A.W. (1986a) Polyamine metabolism and osmotic stress. II. Improvement of oat protoplasts by an inhibitor of arginine decarboxylase. Plant Physiol. 82, 375–378
Tiburcio, A.F., Kaur-Sawhney, R., Galston, A.W. (1986b) Spermine synthase as affected by osmotic stress in oat leaves. Plant Physiol. 80, S-303
Tiburcio, A.F., Masdéu, M.A., Dumortier, F.M., Galston, A.W. (1986c) Polyamine metabolism and osmotic stress. I. Relation to protoplast viability. Plant Physiol. 82, 369–374
Torrigiani, P., Serafini-Fracassini, D., Biondi, S., Bagni, N. (1986) Evidence for the subcellular localization of polyamines and their biosynthetic enzymes in plant cells. J. Plant Physiol. 124, 23–29
Winer, L., Apelbaum, A. (1986) Involvement of polyamines in the development and ripening of avocado fruits. J. Plant Physiol. 26, 223–234
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This research was supported by the Agricultural and Food Research Council and by the British-Spanish joint research programme Acción Integrade HB-079 (R.T.B. and A.F.T.), British Council SPN/BAR/991 (R.T.B.) and Comision Interministerial de Cienica y Tecnologia 90-130 (A.F.T.). We thank Merrell Dow Research Center (Cincinnati, Ohio) for the gift of DFMA and Teresa Capell and Xavier Figueras (Univ. Barcelona) for help and suggestions.
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Besford, R.T., Richardson, C.M., Campos, J.L. et al. Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189, 201–206 (1993). https://doi.org/10.1007/BF00195077
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DOI: https://doi.org/10.1007/BF00195077