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Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa

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Abstract

Centaurea maculosa Lam. is a noxious weed in western North America that produces a phytotoxin, (±)-catechin, which is thought to contribute to its invasiveness. Areas invaded by C. maculosa often result in monocultures of the weed, however; in some areas, North American natives stand their ground against C. maculosa and show varying degrees of resistance to its phytotoxin. Two of these resistant native species, Lupinus sericeus Pursh and Gaillardia grandiflora Van Houtte, were found to secrete increased amounts of oxalate in response to catechin exposure. Mechanistically, we found that oxalate works exogenously by blocking generation of reactive oxygen species in susceptible plants and reducing oxidative damage generated in response to catechin. Furthermore, field experiments show that L. sericeus indirectly facilitates native grasses in grasslands invaded by C. maculosa, and this facilitation can be correlated with the presence of oxalate in soil. Addition of exogenous oxalate to native grasses and Arabidopsis thaliana (L.) Heynh grown in vitro alleviated the phytotoxic effects of catechin, supporting the field experiments and suggesting that root-secreted oxalate may also act as a chemical facilitator for plant species that do not secrete the compound.

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Abbreviations

HPLC:

High pressure liquid chromatography

ROS:

Reactive oxygen species

References

  • Bais HP, Walker TS, Stermitz FR, Hufbauer R, Vivanco JM (2002) Enantiomeric-dependant phytotoxic and antimicrobial activity of (+/−)-catechin: a rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128:1173–1179

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plant invasion: from molecules and genes to species interactions. Science 301:1377–1380

    Article  PubMed  CAS  Google Scholar 

  • Blair AC, Hanson BD, Brunk GR, Marrs RA, Westra P, Nissen SJ, Hufbauer RA (2005) New techniques and findings in the study of a candidate allelochemical implicated in invasion success. Ecol Lett 8:1039–1047

    Article  Google Scholar 

  • Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbours: a mechanism for exotic invasion. Science 290:521–523

    Article  PubMed  CAS  Google Scholar 

  • Callaway RM, Deluca TH, Belliveau WM (1999) Biological control herbivores may increase competitive ability of the noxious weed Centaurea maculosa. Ecology 80:1196–1201

    Google Scholar 

  • Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE (2004) Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology 85:1062–1071

    Article  Google Scholar 

  • Coppola ED, Starr MS (1986) Liquid chromatographic determination of major organic acids in apple juice and cranberry juice cocktail: collaborative study. J Assoc Off Anal Chem 69:594–598

    CAS  Google Scholar 

  • Cruz-Ortega R, Ayala-Cordero G, Anaya AL (2002) Allelochemical stress produced by the aqueous leachate of Callicarpa acuminata: effects on roots of bean, maize, and tomato. Physiol Plant 116:20–27

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Gardner WK, Barber DA, Parbery DG (1983) The acquisition of phosphorus by Lupinus alba L.: II. The probable mechanism by which phosphorus movement in the soil/root interface is enhanced. Plant Soil 70:107–124

    Article  CAS  Google Scholar 

  • Green MA, Fry SC (2005) Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-l-threonate. Nature 433:83–87

    Article  PubMed  CAS  Google Scholar 

  • Hammondkosak KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791

    Article  Google Scholar 

  • Hopper W, Mahadevan A (1997) Degradation of catechin by Bradyrhizobium japonicum. Biodegradation 8:159–165

    Article  CAS  Google Scholar 

  • Kaim W, Schwederski B (1994) Bioinorganic chemistry: inorganic elements in the chemistry of life. Wiley, New York

    Google Scholar 

  • Kayashima T, Katayama T (2002) Oxalate is available as a natural antioxidant in some systems. Biochem Biophys Acta 1537:1–3

    Google Scholar 

  • Keerthisinghe G, Hocking PJ, Ryan PR, Delhaize E (1998) Effect of phosphorus supply on the formation and function of proteid roots of white lupine (Lupinus albus L.). Plant Cell Environ 21:467–478

    Article  CAS  Google Scholar 

  • Libert B, Franceschi VR (1980) Oxalate in crop plants. J Agric Food Chem 35:926–938

    Article  Google Scholar 

  • Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol 38:1019–1025

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassay with tissue culture. Physiol Plant 15:473

    Article  CAS  Google Scholar 

  • Neumann G, Massonneau A, Martinoia E, Römheld V (1999) Physiological adaptations to phosphorus deficiency during proteoid root development in white lupine. Planta 208:373–328

    Article  CAS  Google Scholar 

  • Palgi N, Vatnik I, Pinshow B (2005) Oxalate, calcium and ash intake and excretion balances in fat sand rats (Psammomys obesus) feeding on two different diets. Compar Biochem Physiol DOI 10.1016/j.cbpb.2005.03.011

  • Perry LG, Thelen GC, Ridenour WM, Weir TL, Callaway RM et al (2005) Dual role for an allelochemical: (+/−)-catechin from Centaurea maculosa root exudates regulates conspecific seedling establishment. J Ecol 93:1126–1135

    Article  CAS  Google Scholar 

  • Recknagel RO, Glende EA (1984) Spectrophotometric detection of lipid conjugated dienes. Method Enzymol 105:331–337

    Article  CAS  Google Scholar 

  • Ridenour WM, Callaway RM (2001) The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 124:444–450

    Article  Google Scholar 

  • Ridenour WM, Callaway RM (2003) Root herbivores, pathogenic fungi, and competition between Centaurea maculosa and Festuca idahoensis. Plant Ecol 169:161–170

    Article  Google Scholar 

  • Ryan PR, Delhaize E, Randall PJ (1995) Malate efflux from root apices and tolerance to aluminum are highly correlated in wheat. Aust J Plant Physiol 22:531–563

    Article  CAS  Google Scholar 

  • Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhrb R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in lycopersicon esculentum. Plant Cell 16:616–628

    Article  PubMed  CAS  Google Scholar 

  • Stermitz FR, Bais HP, Foderaro TA, Vivanco JM (2003) 7,8-Benzoflavone: a phytotoxin from root exudates of invasive Russian knapweed. Phytochemistry 64:493–497

    Article  PubMed  CAS  Google Scholar 

  • Thelen GC, Vivanco JM, Newingham B, Good W, Bais HP et al (2005) Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives. Ecol Lett 8:209–217

    Article  Google Scholar 

  • Tiwari BS, Belenghi B, Levine A (2002) Oxidative stress increased respiration and generation of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol 128:1271–1281

    Article  PubMed  CAS  Google Scholar 

  • Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292

    Article  Google Scholar 

  • Weir TL, Bais HP, Vivanco JM (2003) Intraspecific and interspecific interactions mediated by a phytotoxin, (−)-catechin, secreted by the roots of Centaurea maculosa (spotted knapweed). J Chem Ecol 29:2397–2412

    Article  PubMed  CAS  Google Scholar 

  • Weir TL, Park S-W, Vivanco JM (2004) Biochemical and physiological mechanisms mediated by allelochemicals. Curr Opin Plant Biol 7:472–479

    Article  PubMed  CAS  Google Scholar 

  • Yan F, Zhu YY, Muller C, Zorb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol 129:50–63

    Article  PubMed  CAS  Google Scholar 

  • Yang JC, Loewus FA (1975) Metabolic conversion of l-ascorbic-acid to oxalic-acid in oxalate-accumulating plants. Plant Physiol 56:283–285

    Article  PubMed  CAS  Google Scholar 

  • Yang YY, Jung JY, Song WY, Suh HS, Lee Y (2000) Identification of rice varieties with high tolerance or sensitivity to lead and characterization of the mechanism of tolerance. Plant Physiol 124:1019–1026

    Article  PubMed  CAS  Google Scholar 

  • Yu JQ, Ye SF, Zhang MF, Hu WH (2003) Effects of root exudates and aqueous root extracts of cucumber (Cucumis sativus) and allelochemicals, on photosynthesis and antioxidant enzymes in cucumber. Biochem Syst Ecol 31:129–139

    Article  CAS  Google Scholar 

  • Zacchini M, Agazio M (2004) Spread of oxidative damage and antioxidative responses through cell layers of tobacco callus after UV-C treatment. Plant Physiol Biochem 42:445–450

    Article  PubMed  CAS  Google Scholar 

  • Zheng SJ, Ma MF, Matsumoto H (1998) High aluminum resistance in buckwheat: I. Al-induced specific secretion of oxalate from root tips. Plant Physiol 117:745–751

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from USDA-WRIPM (grant no. 2003-05060, J.M.V.), National Science Foundation- (grant no. NSF-IBN 0335203, J.M.V.), U.S. Department of Defense SERDP (CS1388 to J.M.V. and R.M.C.) and Invasive Weeds Initiative of the State of Colorado (J.M.V. and F.R.S.). JMV is an NSF-CAREER faculty fellow (grant no. MCB 093014).

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Correspondence to Jorge M. Vivanco.

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Weir, T.L., Bais, H.P., Stull, V.J. et al. Oxalate contributes to the resistance of Gaillardia grandiflora and Lupinus sericeus to a phytotoxin produced by Centaurea maculosa . Planta 223, 785–795 (2006). https://doi.org/10.1007/s00425-005-0192-x

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