Abstract
Treatment of barley seeds (Hordeum vulgare L.) with streptomycin, an inhibitor of plastid protein synthesis, resulted in growth of the albino phenotype seedlings with ribosome-deficient undifferentiated plastids and chlorophyll (Chl) level as low as 0.1% of that in control plant leaves. A major effect of the antibiotic was almost complete suppression of the ability of plants to synthesize 5-aminolevulinic acid (ALA) intended for Chl biosynthesis. The activity of synthesis of ALA intended for heme porphyrin biosynthesis in etiolated and greening seedlings and in light-grown albinophenotype plants was insensitive to light and cytokinins. In the upper parts of leaves of streptomycin-treated plants, exhibiting 60% Chl deficit, the cells with three types of chloroplasts could be observed: normally developed chloroplasts, chloroplasts composed of single thylakoids and grana, and completely undifferentiated plastids. In this Chl-deficient tissue, ALA synthesis was found to be stimulated by kinetin but much less than in leaves of the control plants. The endogenous cytokinin content in etiolated and greening seedlings treated with streptomycin was almost the same as it was in untreated control seedlings. The cytokinin level in the white tissue of plants grown in the light was on average twice as high as that in green leaves of the control plants. The capability of kinetin to stimulate the synthesis of ALA used for Chl biosynthesis was found to correlate with the Chl content and organization of the chloroplast internal structure. This correlation confirms the hypothesis that the normally developed internal structure of plastids is essential for the adequate phytohormone response in plants.
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Abbreviations
- ALA:
-
5-aminolevulinic acid
- Chl:
-
chlorophyll
- LA:
-
levulinic acid
References
Khokhlova, V.A., Sveshnikova, I.N., and Kulaeva, O.N., Effects of Phytohormones on Formation of Chloroplast Structure in Isolated Pumpkin Seedlings, Tsitologiya, 1971, vol. 13, pp. 1074–1078.
Chory, J., Reinecke, D., Sim, S., Washburn, T., and Brenner, M., A Role for Cytokinins in De-Etiolation in Arabidopsis (det Mutants Have an Altered Response to Cytokinins), Plant Physiol., 1994, vol. 104, pp. 339–347.
Serve, B.T., Axelos, M., and Peaud-Lenoel, C., Cytokinins Modulate the Expression of Genes Encoding the Protein of the Light-Harvesting Chlorophyll a/b Complex, Plant. Mol. Biol., 1985, vol. 5, pp. 155–163.
Flores, S. and Tobin, E.M., Benzyladenine Modulation of the Expression of Two Genes for Nuclear-Encoded Chloroplast Proteins in Lemna gibba: Apparent Post-Transcriptional Regulation, Planta, 1986, vol. 168, pp. 340–349.
Ohya, T. and Suzuki, H., The Effect of Benzyladenine on the Accumulation of Messenger RNAs That Encode the Large and Small Subunits of Rubisco and Light Harvesting Chlorophyll a/b-Protein in Excised Cucumber Cotyledons, Plant Cell Physiol., 1991, vol. 32, pp. 577–580.
Kusnetsov, V.V., Oelmüller, R., Sarwat, M.I., Porfirova, S.A., Cherepneva, G.N., Herrmann, R.G., and Kulaeva, O.N., Cytokinin, Abscisic Acid and Light Affect Accumulation of Chloroplast Proteins in Lupinus luteus Cotyledons without Notable Effect on Steady-State mRNAs Levels, Planta, 1994, vol. 194, pp. 318–327.
Sigiura, M., Promotion of Chlorophyll Synthesis by Kinetin, Bot. Mag. (Tokyo), 1963, vol. 76, pp. 309–310.
Averina, N.G. and Shlyk, A.A., Effect of Kinetin on Accumulation and Activity of Protochlorophyllide in Etiolated and Post-Etiolated Barley Leaves, Sov. Plant Physiol., 1972, vol. 19, pp. 487–496.
Fletcher, R., Teo, S., and Alt, A., Stimulation of Chlorophyll Synthesis in Cucumber Cotyledons by Benzyladenine, Can. J. Bot., 1973, vol. 51, pp. 937–939.
Kusnetsov, V.V., Herrmann, R.G., Kulaeva, O.N., and Oelmüller, R., Cytokinin Stimulates and Abscisic Acid Inhibits Greening of Etiolated Lupinus luteus Cotyledons by Affecting the Expression of the Light-Sensitive Protochlorophyllide Oxidoreductase, Mol. Gen. Genet., 1998, vol. 259, pp. 21–28.
Masuda, T., Ohta, H., Shioi, Y., Tsuji, H., and Takamiya, K., Stimulation of Glutamyl-tRNA Reductase Activity by Benzyladenine in Greening Cucumber Cotyledons, Plant Cell Physiol., 1995, vol. 36, pp. 1237–1243.
Vershilovskaya, I.V., Yaronskaya, E.B., Vezitskii, A.Yu., and Averina, N.G., Investigation of Cytokinin Action Mechanisms on the System of Chlorophyll Biosynthesis, Izv. Nat. Akad. Nauk Belarusi, Ser. Biol. nauk, 2004, no. 1, pp. 80–84.
Kulaeva, O.N., Burkhanova, E.A., Karavaiko, N.N., Selivankina, S.Y., Porfirova, S.A., Maslova, G.G., Zemlyachenko, Y.V., and Börner, T., Chloroplasts Affect the Leaf Response to Cytokinin, J. Plant Physiol., 2002, vol. 159, pp. 1309–1316.
Zubko, M.K. and Day, A., Stable Albinism Induced without Mutagenesis: A Model for Ribosome-Free Plastid Inheritance, Plant J., 1998, vol. 15, pp. 265–271.
Zubko, M.K. and Day, A., Differential Regulation of Genes Transcribed by Nucleus-Encoded Plastid RNA Polymerase, and DNA Amplification, within Ribosome-Deficient Plastids in Stable Phenocopies of Cereal Albino Mutants, Mol. Gen. Genomics, 2002, vol. 267, pp. 27–37.
Demmig-Adams, B. and Adams, W.W., Chlorophyll and Carotenoid Composition in Leaves of Euonymus kiautschovicus Acclimated to Different Degrees of Light Stress in the Field, Aust. J. Plant Physiol., 1996, vol. 23, pp. 649–659.
Miller, G.W., Denney, A., Wood, J.K., and Welkie, G.W., Light-Induced delta-Aminolevulinic Acid in Dark-Grown Barley Seedlings, Plant Cell Physiol., 1979, vol. 20, pp. 131–143.
Mauzerall, D. and Granick, S., The Occurrence and Determination of 5-Aminolevulinic Acid and Porphobilinogen in Urine, J. Biol. Chem., 1956, vol. 219, pp. 435–446.
Lezhneva, L.A., Rassadina, V.V., Yaronskaya, E.B., Radyuk, M.S., Taran, S.F., and Averina, N.G., Activity of the Fe-Branch of Tetrapyrrole Biosynthesis in the Chlorophyll-Deficient Plastome Mutant of Sunflower (Helianthus annuus L.), Russ. J. Plant Physiol., 2001, vol. 48, pp. 57–61.
Moskaleva, O.V. and Karavaiko, N.N., Dynamics of Endogenous Phytohormones during Development of Maize Seedlings, Sov. Plant Physiol., 1990, vol. 37, pp. 1113–1120.
Kudoyarova, G.R., Veselov, S.Yu., Karavaiko, N.N., Gyuli-zade, V.Z., Cheredova, E.P., Mustafina, A.R., Moshkov, I.E., and Kulaeva, O.N., Immunoenzymatic Test-System for Cytokinin Determination, Sov. Plant Physiol., 1990, vol. 37, pp. 193–199.
Beale, S.I. and Castelfranco, P.A., The Biosynthesis of δ-Aminolevulinic Acid in Higher Plants: I. Accumulation of δ-Aminolevulinic Acid in Greening Plant Tissues, Plant Physiol., 1974, vol. 53, pp. 291–296.
Yaronskaya, E., Ziemann, V., Walter, G., Averina, N., Börner, T., and Grimm, B., Metabolic Control of the Tetrapyrrole Biosynthetic Pathway for Porphyrin Distribution in the Barley Mutant albostrians, Plant J., 2003, vol. 35, pp. 512–522.
Papenbrock, J. and Grimm, B., Regulatory Network of Tetrapyrrole Biosynthesis — Studies for Intracellular Signaling Involved in Metabolic and Developmental Control of Plastids, Planta, 2001, vol. 213, pp. 667–681.
Surpin, M., Larkin, R.M., and Chory, J., Signal Transduction between the Chloroplast and the Nucleus, Plant Cell, 2002, vol. 14,Suppl., pp. S327–S338.
Bougri, O. and Grimm, B., Members of a Low-Copy Number Gene Family Encoding Glutamyl-tRNA Reductase Are Differentially Expressed in Barley, Plant J., 1996, vol. 9, pp. 867–878.
Tanaka, R., Yoshida, K., Nakayashiki, T., Masuda, T., Tsuji, H., Inokuchi, H., and Tanaka, A., Differential Expression of Two hemA mRNAs Encoding Glutamyl-tRNA Reductase Proteins in Greening Cucumber Seedlings, Plant Physiol., 1996, vol. 110, pp. 1223–1230.
Tanaka, R., Yoshida, K., Nakayashiki, T., Tsuji, H., Inokuchi, H., Okada, K., and Tanaka, A., The Third Member of the hemA Gene Family Encoding Glutamyl-tRNA Reductase Is Primarily Expressed in Roots in Hordeum vulgare, Photosynth. Res., 1997, vol. 53, pp. 161–171.
Yaronskaya, E.B., Vershilovskaya, I.V., and Averina, N.G., Effect of Kinetin on Activity of Heme Branch of Tetrapyrrole Biosynthesis in Hordeum vulgare L. Seedlings, Izv. Nat. Akad. Nauk Belarusi, Ser. Biol. nauk, 2004, no. 2, pp. 79–82.
Kof, E.M., Kefeli, V.I., Kutachek, M., Eder, I., Chermak, V., and Gostimskii, S.A., The Effects of Mutation-Induced Chlorophyll Deficiency and Light on Phytohormones in Pea Plants, Russ. J. Plant Physiol., 1994, vol. 41, pp. 592–598.
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Original Russian Text © E.B. Yaronskaya, E.R. Griskevich, N.L. Trukhanovets, N.G. Averina, 2007, published in Fiziologiya Rastenii, 2007, Vol. 54, No. 3, pp. 440–448.
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Yaronskaya, E.B., Gritskevich, E.R., Trukhanovets, N.L. et al. Effect of kinetin on early stages of chlorophyll biosynthesis in streptomycin-treated barley seedlings. Russ J Plant Physiol 54, 388–395 (2007). https://doi.org/10.1134/S1021443707030144
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DOI: https://doi.org/10.1134/S1021443707030144