Tagetitoxin affects plastid development in seedling leaves of wheat Article Received: 02 October 1984 Accepted: 11 March 1985 DOI:
Cite this article as: Lukens, J.H. & Durbin, R.D. Planta (1985) 165: 311. doi:10.1007/BF00392227 Abstract
Ultrastructural and biochemical approaches were used to investigate the mode of action of tagetitoxin, a nonhost-specific phytotoxin produced by
Pseudomonas syringae pv. tagetis (Hellmers) Young, Dye and Wilkie, which causes chlorosis in developing — but not mature — leaves. Tagetitoxin has no effect on the growth rate or morphology of developing leaves of wheat ( Triticum aestivum L.) seedlings. Its cytological effects are limited to plastid aberrations; in both light-and dark-grown leaves treated with toxin, internal plastid membranes fail to develop normally and plastid ribosomes are absent, whereas mitochondrial and cytoplasmic ribosomes are unaffected. The activity of a plastid stromal enzyme, ribulose-1,5-bisphosphate carboxylase (RuBPCase, EC 220.127.116.11), which is co-coded by nuclear and chloroplast genes, is markedly lower in extracts of both light-and dark-grown toxin-treated leaves, whereas the activity of another stromal enzyme, NADP-glyceraldehyde-3-phosphate dehydrogenase (NADP-G-3P-DH, EC 18.104.22.168), which is coded only by the nuclear genome, is significantly lower in extracts of light-grown, but not of dark-grown, treated leaves. The mitochondrial enzymes fumarase (EC 22.214.171.124) and cytochrome- c oxidase (EC 126.96.36.199) are unaffected by toxin in dark-grown leaves, but fumarase activity is reduced in light-grown ones. Four peroxisomal enzyme activities are lowered by toxin treatment in both light- and dark-grown leaves. Light- and dark-grown, toxintreated leaves contain about 50% and 75%, respectively, of the total protein of untreated leaves. There are threefold and twofold increases in free amino acids in light-grown and dark-grown treated leaves, respectively. In general, the effects of tagetitoxin are more extensive and exaggerated in light-grown than in dark-grown leaves. We conclude that tagetitoxin interferes primarily with a light-independent aspect of chloroplast-specific metabolism which is important in plastid biogenesis. Key words Chloroplast development Chloroplast ribosomes Etioplast (prolamellar body) Pseudomonas (toxin) Tagetitoxin Triticum (chloroplast development) Abbreviations NADP-G-3-DH
shikimic acid dehydrogenase
Beevers, H. (1979) Microbodies in higher plants. Annu. Rev. Plant. Physiol.
Bieleski, R.L., Turner, N.A. (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal. Biochem.
Blair, G.E., Ellis, R.J. (1973) Protein synthesis in chloroplasts. I. Light-driven synthesis of the large subunit of Fraction I protein by isolated pea chloroplasts. Biochim. Biophys. Acta
Boller, T., Kende, H. (1979) Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol.
Bradford, M.M. (1976) A rapid and sensitive method for quantitation of μg quantities of protein using the principle of protein-dye binding. Anal. Biochem.
Castelfranco, P.A., Beale, S.I. (1981) Chlorophyll biosynthesis. In: Stumpf, P.K., Conn, E.E., eds. The biochemistry of plants, vol. 8, pp. 375–421, Academic Press, New York London
Dean, C., Leech, R.M. (1982) Genome expression during normal leaf development. I. Cellular and chloroplast numbers and DNA, RNA, and protein levels in tissues of different ages within a seven day old wheat leaf. Plant Physiol.
De Boer, J., Feierabend, J. (1974) Comparison of the effects of cytokinins on enzyme development in different cell compartments of the shoot organs of rye seedlings. Z. Pflanzenphysiol.
Ellis, R.J., Hartley, M.R. (1971) Sites of synthesis of chloroplast proteins. Nature New Biol.
Eyster, H.C. (1950) Catalase activity in pigment-deficient types of corn. Plant Physiol.
Fedtke, C. (1982) Biochemistry and physiology of herbicide action, Springer, New York Heidelberg Berlin
Feierabend, J. (1975) Developmental studies on microbodies in wheat leaves. III. On the photocontrol of microbody development. Planta
Feierabend, J. (1977) Capacity for chlorophyll synthesis in heat-bleached 70S ribosome-deficient rye leaves. Planta
Feierabend, J., Beevers, H. (1972a) Developmental studies on microbodies in wheat leaves. I. Conditions influencing enzyme development. Plant Physiol.
Feierabend, J., Beevers, H. (1972b) Developmental studies on microbodies in wheat leaves. II. Ontogeny of particulate enzyme associations. Plant Physiol.
Feierabend, J., Brassel, D. (1977) Subcellular localization of shikimate dehydrogenase in higher plants. Z. Pflanzenphysiol.
Feierabend, J., Kemmerich, P. (1983) Mode of interference of chlorosis-inducing herbicides with peroxisomal enzyme activities. Physiol. Plant.
Feierabend, J., Mikus, M. (1977) Occurrence of a high temperature sensitivity of chloroplast ribosome formation in several higher plants. Plant Physiol.
Feierabend, J., Schrader-Reichhardt, U. (1976) Biochemical differentiation of plastids and other organelles in rye leaves with a high temperature-induced deficiency of plastid ribosomes. Planta
Feierabend, J., Schubert, B (1978) Comparative investigation of the action of several chlorosis-inducing herbicides on the biogenesis of chloroplasts and leaf microbodies. Plant Physiol.
George, P. (1953) Intermediate compound formation with peroxidase and strong oxidizing agents. J. Biol. Chem.
Griffiths, W.T., Beer, N.S. (1982) Site of synthesis of NADPH protochlorophyllide oxidoreductase in rye (
). Plant Physiol.
Grob, K., Matile P (1980) Compartmentation of ascorbic acid in vacuoles of horseradish root cells. Z. Pflanzenphysiol.
Gruber, P.J., Becker, W.M., Newcomb, E. (1972) The occurrence of microbodies and peroxisomal enzymes in achlorophyllous leaves. Planta
Jutte, S.M., Durbin, R.D. (1979) Ultrastructural effects in zinnia leaves of a chlorosis-inducing toxin from
Lee, T.T. (1973) On extraction and quantitation of plant peroxidase isoenzymes. Physiol. Plant.
Lück, H. (1965) Catalase. In: Bergmeyer, H.U., ed. Methods of enzymatic analysis, pp. 885–894, Academic Press, New York London
Lukens, J.H. (1983) Investigations into the mode of action of tagetitoxin in plants. Ph.D. thesis, University of Wisconsin, Madison, USA
Mitchell, R.E., Bieleski, R.L. (1977) Involvement of phaseolotoxin in the halo blight of beans. Plant Physiol.
Mitchell, R.E., Durbin, R.E. (1981) Tagetitoxin, a toxin produced by
: purification and partial characterization. Physiol. Plant Pathol
Mitchell, R.E., Hart, P.A. (1983) The structure of tagetitoxin, a phytotoxin of
Müller, B., Ziegler, I., Ziegler, H. (1969) Lichtinduzierte, reversible Aktivitätssteigerung der NADP-abhängigen Glycerinaldehyd-3-Phosphatdehydrogenase in Chloroplasten. Zum Mechanismus der Reaktion. Eur. J. Biochem.
Nadolny, L. (1978) The involvement of peroxidase in protection of tobacco against the hypersensitive reaction induced by the
B1 isolate. M.S. thesis, University of Wisconsin, Madison, USA
Nilsson, G. (1978) Effects of glyphosate on the amino acid content in spring wheat plants. Weed Abstr.
Racker, E. (1962) Ribulose diphosphate carboxylase from spinach leaves. Methods Enzymol.
Reiss, T., Bergfeld, R., Link, G., Thien, W., Mohr, H. (1983) Photooxidative destructive of chloroplasts and its consequences for cytosolic enzyme levels and plant development. Planta
Steinrücken, H.C., Amrhein, N. (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem. Biophys. Res. Commun.
Styer, D.J., Durbin, R.D. (1982a) Common ragweed: a new host for
. Plant Dis.
Styer, D.J., Durbin, R.D. (1982b) Isolation of
from sunflower in Wisconsin. Plant Dis.
Tolbert, N.E., Oeser, A., Kisacki, T., Hageman, R.H., Yamazaki, R.K. (1968) Peroxisomes from spinach leaves containing enzymes related to glycolate metabolism. J. Biol. Chem.
Trimboli, D., Fahy, P.C., Baker, K.F. (1978) Apical chlorosis and leaf spot of
spp. caused by
Hellmers. Aust. J. Agric. Res.
Wintermans, J.F.G.M., De Mots, A. (1965) Spectrophotometric characteristics of chlorophyll
and their pheophytins in ethanol. Biochim. Biophys. Acta