Skip to main content
SpringerLink
Log in

Juglone Disrupts Root Plasma Membrane H+-ATPase Activity and Impairs Water Uptake, Root Respiration, and Growth in Soybean (Glycine max) and Corn (Zea mays)

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Juglone is phytotoxic, but the mechanisms of growth inhibition have not been fully explained. Previous studies have proposed that disruption of electron transport functions in mitochondria and chloroplasts contribute to observed growth reduction in species exposed to juglone. In studies reported here, corn and soybean seedlings grown in nutrient solution amended with 10, 50, or 100 μM juglone showed significant decreases in root and shoot dry weights and lengths with increasing concentrations. However, no significant differences in leaf chlorophyll fluorescence or CO2-dependent leaf oxygen evolution were observed, even in seedlings that were visibly affected. Disruption of root oxygen uptake was positively correlated with increasing concentrations of juglone, suggesting that juglone may reach mitochondria in root cells. Water uptake and acid efflux also decreased for corn and soybean seedlings treated with juglone, suggesting that juglone may affect metabolism of root cells by disrupting root plasma membrane function. Therefore, the effect of juglone on H+-ATPase activity in corn and soybean root microsomes was tested. Juglone treatments from 10 to 1000 μM significantly reduced H+-ATPase activity compared to controls. This inhibition of H+-ATPase activity and observed reduction of water uptake offers a logical explanation for previously documented phytotoxicity of juglone. Impairment of this enzyme's activity could affect plant growth in a number of ways because proton-pumping in root cells drives essential plant processes such as solute uptake and, hence, water uptake.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Babakov, A. V., Chelysheva, V. V., Klychnikov, O. I., Zorinyanz, S. E., Trofimova, M. S., and De Boer, A. H. 2000. Involvement of 14-3-3 proteins in the osmotic regulation of H+-ATPase in plant plasma membranes. Planta 211:446–448.

    Google Scholar 

  • Barkosky, R. R., Butler, J. L., and Einhellig, F. A. 1999. Mechanisms of hydroquinone-induced growth reduction in leafy spurge. J. Chem. Ecol. 25:1611–1621.

    Google Scholar 

  • Barkosky, R. R., Einhellig, F. A., and Butler, J. L. 2000. Caffeic acid-induced changes in plant-water relationships and photosynthesis in leafy spurge. J. Chem. Ecol. 26:2095–2109.

    Google Scholar 

  • Blein, J. P., Bourdil, I., Rossignol, M., and Scalla, R. 1988. Cerospora beticola toxin inhibits vanadate-sensitive H+ transport in corn root membrane vesicles. Plant Physiol. 88:429–434.

    Google Scholar 

  • Briskin, D. P. and Hanson, J. B. 1992. How does the plant plasma membrane H+-ATPase pump protons? J. Exp. Bot. 43:269–289.

    Google Scholar 

  • Brooks, M. G. 1951. Effects of black walnut trees and their products on the vegetation. Agricultural Extension State Bulletin No. 347. West Virginia University, Morgantown, WV.

    Google Scholar 

  • Cai, L., Wei, G. X., van der Bijl, P., and Wu, C. D. 2000. Namibian chewing stick, Diospyros lycioides, contains antibacterial compounds against oral pathogens. J. Agric. Food Chem. 48:909–914.

    Google Scholar 

  • Calera, M. R., Anaya, A. L., and Gavilanes-Ruiz, M. 1995. Effect of phytotoxic resin glycoside on activity of H+-ATPase from plasma membrane. J. Chem. Ecol. 21:289–287.

    Google Scholar 

  • Che, F. S., Kasamo, K., Fukuchi, N., Isogai, A., and Suzuki, A. 1992. Bacterial phytotoxins, syringomycin, syringostatin and syringotoxin, exert their effect on plasma membrane H+-ATPase partly by a detergent-like action and partly by inhibition of the enzyme. Physiol. Plant 86:518–524.

    Google Scholar 

  • Crane, F. I. and Møller, I. M. 1988. Plasmalemma redox functions in plants. Physiol. Plant 73:161–200.

    Google Scholar 

  • Davis, E. F. 1928. The toxic principle of Juglans nigra as identified with synthetic juglone and its toxic effects on tomato and alfalfa plants. Am. J. Bot. 15:620.

    Google Scholar 

  • Dawson, J. O. and Seymour, P. E. 1983. Effects of juglone concentration on growth in vitro of Frankia Ar13 and Rhizobium japonicum strain 71. J. Chem. Ecol. 9:1175–1183.

    Google Scholar 

  • Delieu, T. and Walker, D. A. 1981. Polarographic measure of photosynthetic oxygen evolution by leaf discs. New Phytol. 89:165–178.

    Google Scholar 

  • De Scisciolo, B., Leopold, D. J., and Walton, D. C. 1990. Seasonal patterns of juglone in soil beneath Juglans nigra (black walnut) and influence of J. nigra on understory vegetation. J. Chem. Ecol. 16:1111–1130.

    Google Scholar 

  • Di Giorgio, D., Camoni, L., and Ballio, A. 1994. Toxins of Pseudomonas syringae pv. syringae affect H+-transport across the plasma membrane in maize. Physiol. Plant 91:741–746.

    Google Scholar 

  • DÖring, O., Lüthje, S., and BÖttger, M. 1992a. Inhibitors of the plasma membrane redox system of Zea mays L. roots. The vitamin K antagonists dicumarol and warfarin. Biochem. Biophys. Acta 1110:235–238.

    Google Scholar 

  • DÖring, O., Lüthje, S., and BÖttger, M. 1992b. Modification of the activity of the plasma membrane redox system of Zea mays L. roots by vitamin K3 and dicumarol. J. Exp. Bot. 43:175–181.

    Google Scholar 

  • Duroux, L., Delmotte, F. M., Lancelin, J. M., Keravis, G., and Jay, A. C. 1998. Insight into naphthoquinone metabolism: beta-glucosidase-catalyzed hydrolysis of hydrojuglone beta-D-glucopyranoside. Biochem. J. 333:275–283.

    Google Scholar 

  • Einhellig, F. A. 1995. Mechanism of action of allelochemicals in allelopathy, pp. 96–116, in K. M. Inderjit, M. Dakshini, and F. A. Einhellig (eds.). Allelopathy: Organisms, Processes, and Applications. ACS Symposium Series 582, American Chemical Society, Washington, DC.

    Google Scholar 

  • Einhellig, F. A. and Souza, I. F. 1992. Phytotoxicity of sorgoleone found in grain sorghum root exudates. J. Chem. Ecol. 18:1–11.

    Google Scholar 

  • Fedtke, C. 1993. Rooting and algal tests for herbicide mode of action studies, pp. 239–250, in P. BÖger and G. Sandmann (eds.). Target Assays for Modern Herbicides and Related Phytotoxic Compounds. Lewis Publishers, Ann Arbor, MI.

    Google Scholar 

  • Friebe, A., Roth, U., Kück, P., Schnabl, H., and Schulz, M. 1997. Effects of 2,4-dihydroxy-1,4-benzoxazin-3-ones on the activity of plasma membrane H+-ATPase. Phytochemistry 44:979–983.

    Google Scholar 

  • Funk, D. T., Case, P. J., Rietveld, W. J., and Phares, R. E. 1979. Effects of juglone on the growth of coniferous seedlings. Forest Sci. 25:452–454.

    Google Scholar 

  • Funt, R. C. and Martin, J. 2000. Black Walnut Toxicity to Plants, Humans and Horses. Ohio State University Extension Fact Sheet. HYG-1148–93.

  • Glass, A. D. M. and Dunlap, J. 1974. Influence of phenolic acids on ion uptake. IV. Depolarization of membrane potentials. Plant Physiol. 54:855–858.

    Google Scholar 

  • Gleiter, H. M. and Renger, G. 1993. A simple fluorometric detection of Photosystem II inhibitors, pp. 69–74, in P. BÖger and G. Sandmann (eds.). Target Assays for Modern Herbicides and Related Phytotoxic Compounds. Lewis Publishers, Ann Arbor, MI.

    Google Scholar 

  • Graves, C. H., Hedin, P. A., and Langhans, V. E. 1979. A survey of juglone levels among pecan, hickory, and walnut, pp. 113–121, in Proceedings of the 72nd Annual Convention of SE Growers Assocication. Hilton Head, SC.

  • Hejl, A. M., Einhellig, F. A., and Rasmussen, J. A. 1993. Effects of juglone on growth, photosynthesis, and respiration. J. Chem. Ecol. 19:559–568.

    Google Scholar 

  • Hejl, A. M. and Koster, K. L. 1998. The phytotoxin juglone inhibits microsomal H+-ATPase activity. Plant Physiol. 117(S):66.

    Google Scholar 

  • Hoagland, D. R. and Arnon, D. I. 1950. The water culture method for growing plants without soil. Calif. Agric. Exp. Station Circ. 347.

  • Hull, M. R. and Cobb, A. H. 1998. An investigation of herbicide interaction with the H+-ATPase activity of plant plasma membranes. Pestic. Sci. 53:155–164.

    Google Scholar 

  • Jose, S. and Gillispie, A. R. 1998a. Allelopathy in black walnut (Juglans nigra L.) alley cropping. I. Spatio-temporal variation in soil juglone in a black walnut-corn (Zea mays L.) alley cropping system in the midwestern USA. Plant Soil 203:191–198.

    Google Scholar 

  • Jose, S. and Gillispie, A. R. 1998b. Allelopathy in black walnut (Juglans nigra L.) alley cropping. II. Effects of juglone on hydroponically grown corn (Zea mays L.) and soybean (Glycine max L. Merr.) growth and physiology. Plant Soil 203:199–205.

    Google Scholar 

  • Koeppe, D. E. 1972. Some reactions of isolated corn mitochondria influenced by juglone. Physiol. Plant 27:89–94.

    Google Scholar 

  • Lee, K. C. and Campbell, R. W. 1969. Nature and occurrence of juglone in Juglans nigra L. Hortic. Sci. 4:297–298.

    Google Scholar 

  • Lüthje, S., Van Gestelen, P., Cordoba-Pedregosa, M. C., Gonzalez-Reyes, J. A., Asard, H., Villalba, J. M., and BÖttger, M. 1998. Quinones in plant plasma membranes: A missing link? Protoplasma 205:43–51.

    Google Scholar 

  • MacDaniels, L. H. and Pinnow, D. L. 1976. Walnut toxicity, an unsolved problem. North Nut Growth Assoc. Annu. Rep. 31:172–179.

    Google Scholar 

  • Magiri, E. N., Konji, V. N., Makawiti, D. W., and Midiwo, J. 1995. Effect of plant quinones on insect flight muscle mitochondria. Insect Sci. Appl. 16:183–189.

    Google Scholar 

  • Massey, A. B. 1925. Antagonism of the walnuts (Juglans nigra L. and J. cinerea L.) in certain plant associations. Phytopathology 15:773–784.

    Google Scholar 

  • Meazza, G., Scheffler, B. E., Tellez, M. R., Rimando, A. M., Nanayakkara, N. P. D., Khan, I. A., Abourashed, E. A., Romagni, J. G., Duke, S. O., and Dayan, F. E., 2002. The inhibitory activity of natural products on plant p-hydroxyphenylpyruvate dioxygenase. Phytochemistry 59:281–288.

    Google Scholar 

  • Michelet, B. and Boutry, M. 1995. The plasma membrane H+-ATPase. Plant Physiol. 108:1–6.

    Google Scholar 

  • Morré, D. J., Brightman, A. O., Wu, L. Y., Barr, R., Leak, B., and Crane, F. L. 1988. Role of plasma membrane redox activities in elongation growth in plants. Physiol. Plant 73:187–193.

    Google Scholar 

  • Ögren, E. and Baker, N. R. 1985. Evaluation of a technique for the measurement of chlorophyll fluorescence from leaves exposed to continuous white light. Plant Cell Environ. 8:539–547.

    Google Scholar 

  • Öllinger, K. and Brunmark, A. 1991. Effect of hydroxy substituent position on 1,4-naphthoquinone toxicity to rat hepatocytes. J. Biol. Chem. 266:21496–21503.

    Google Scholar 

  • Peñuelas, J., Ribas-Carbo, M., and Giles, L. 1996. Effects of allelochemicals on plant respiration and oxygen isotope fractionation by the alterative oxidase. J. Chem. Ecol. 22:801–805.

    Google Scholar 

  • Perry, S. F. 1967. Inhibition of respiration by juglone in Phaseolus and Lycopersicon. Bull. Torrey Bot. Club 94:26–30.

    Google Scholar 

  • Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83:364–356.

    Google Scholar 

  • Peterson, G. L. 1978. A simplified method for analysis of inorganic phosphate in the presence of interfering substances. Anal. Biochem. 84:164–172.

    Google Scholar 

  • Peterson, R. B., Sivak, M. M., and Walker, D. A. 1988. Relationship between steady-state fluorescence yield and photosynthetic efficiency in spinach leaf tissue. Plant Physiol. 88:158–163.

    Google Scholar 

  • Ponder, F., Jr. and Tadros, S. H. 1985. Juglone concentration in soil beneath black walnut interplanted with nitrogen-fixing species. J. Chem. Ecol. 11:937–942.

    Google Scholar 

  • Rietveld, W. J. 1983. Allelopathic effects of juglone on germination and growth of several herbaceous and woody species. J. Chem. Ecol. 9:295–307.

    Google Scholar 

  • Rietveld, W. J., Schlesinger, R. C., and Kessler, K. J. 1983. Allelopathic effects of black walnut on European black alder coplanted as a nurse species. J. Chem. Ecol. 9:1119–1133.

    Google Scholar 

  • Schmidt, S. D. 1988. Degradation of juglone by soil bacteria. J. Chem. Ecol. 14:1561–1571.

    Google Scholar 

  • Seifert, J. R. 1991. Agroforestry: The southern Indiana experience of growing oak, walnut, corn, and soybeans, p. 70, in P. Williams (ed.). Agroforestry in North America. Min. Agric. Food. Ontario, Canada.

  • Sparla, F., Preger, V., Pupillo, P., and Trost, P. 1999. Characterization of a novel NADH-specific, FAD-containing, soluble reductase with ferric citrate reductase activity from maize seedlings. Arch. Biochem. Biophys. 363:301–308.

    Google Scholar 

  • Steudle, E. and Peterson, C. A. 1998. How does water get through roots? J. Exp. Bot. 49:775–788.

    Google Scholar 

  • Thomson, R. H. 1971. Naturally occurring quinones, 2nd edn. Academic Press, New York.

    Google Scholar 

  • Tu, S. I., Patterson, D., Brauer, D., and Hsu, A. F. 1995. Inhibition of corn root membrane ATPase activities by oryzalin. Plant Physiol. Biochem. 33:141–148.

    Google Scholar 

  • Van Duuren, B. L., Segal, A., Tseng, S. S., Rusch, G. M., Loewengart, G., Maté, U., Roth, D., Smith, A., Melchinonne, S., and Seidman, I. 1978. Structure and tumor-promoting activity of analogues of anthralin (1,8-dihydroxy-9-anthrone). J. Med. Chem. 21:26–28.

    Google Scholar 

  • Weidenhamer, J. D. 1996. Distinguishing resource competition and chemical interference: Overcoming the methodological impasse. Agron. J. 88:888–875.

    Google Scholar 

  • Weissenberg, M., Meisner, J., Klein, M., Schaeffler, I., Eliyahu, M., Schmutterer, H., and Ascher, K. R. S. 1997. Effect of substituent and ring changes in naturally occurring naphthoquinones on the feeding response of larvae of Mexican bean beetle, Ephilachna varivestis. J. Chem. Ecol. 23:3–18.

    Google Scholar 

  • Westfall, B. A., Russell, R. L., and Auyong, T. K. 1961. Depressant agent from walnut hulls. Science 134:1617.

    Google Scholar 

  • Zar, J. H. 1996. Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle River, NJ.

    Google Scholar 

  • Zhang, R., Hirsch, O., Mohsen, M., and Samuni, A. 1994. Effects of nitroxide stable radicals on juglone cytotoxicity. Arch. Biochem. Biophys. 312:385–391.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of South Dakota, 414 East Clark Street, Vermillion, South Dakota, 57069, USA

    Angela M. Hejl & Karen L. Koster

Authors
  1. Angela M. Hejl
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen L. Koster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angela M. Hejl.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hejl, A.M., Koster, K.L. Juglone Disrupts Root Plasma Membrane H+-ATPase Activity and Impairs Water Uptake, Root Respiration, and Growth in Soybean (Glycine max) and Corn (Zea mays). J Chem Ecol 30, 453–471 (2004). https://doi.org/10.1023/B:JOEC.0000017988.20530.d5

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:JOEC.0000017988.20530.d5

Search

Navigation