Journal of Chemical Ecology

, Volume 31, Issue 11, pp 2689–2703 | Cite as

Whole Plant Response of Lettuce After Root Exposure to BOA (2(3H)-Benzoxazolinone)



The goal of our work was to expand the knowledge about plant stress response to the allelochemical 2(3H)-benzoxazolinone (BOA). We focused on physiological processes that are affected by this secondary metabolite. Physiological and biochemical characteristics of plants exposed to BOA help us to better understand its mode of action and open the gate to the use of allelochemicals as “natural” herbicides. Measurements on photosynthesis, fluorescence, water relations, antioxidant enzymes (superoxide dismutase, peroxidase), ATPases, and lipid peroxidation indicated that a phytotoxic effect follows BOA exposition. This effect was intense enough to interfere with plant growth and development and to produce “induced senescence.” Based on this, we propose a multifaceted mode of action for BOA with effects at different levels and in different parts of the plant.

Key Words

Allelopathy plants benzoxazolinone mode of action biopesticide allelochemical botanical compound lettuce Lactuca sativa 



The authors are grateful to Drs. Luís González, Nuria Pedrol, and Pilar Ramos, as well as to Ángeles Domínguez, Rosa Bañuelos, Salvador Enguix, Carlos Bolaño, Ana Martínez, Xan X. Santos, and Eva Diéguez for laboratory and technical assistance. We thank also Rocío Cruz Ortega from the Applied and Functional Ecology Department (Ecology Institute), Mexico, for her assistance in the ATPase measurements, and Oliver Weiss for his corrections to the manuscript. This research was supported by the Spanish Ministry of Science and Technology (DGICYT; BFI 2000-0987) and by the Galician Government (PGIDT00 PXI30114PR). Adela Sánchez was financially supported by the Spanish Ministry of Science with a research grant.


  1. Bacon, M. A. 1999The biochemical control of leaf expansion during droughtPlant Growth Regul.29101112CrossRefGoogle Scholar
  2. Bacon, M. A., Wilkinson, S., Davies, W. J. 1998pH-regulated leaf cell expansion in droughted plants is abscisic acid dependentPlant Physiol.11815071515CrossRefPubMedGoogle Scholar
  3. Baerson, R., Sánchez-Moreiras, A., Pedrol-Bonjoch, N., Schulz, M., Kagan, I. A., Agarwal, A. K., Reigosa, M. J., and Duke, S. O. 2005. Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one (BOA). J. Chem. Biol. 1–37, April.Google Scholar
  4. Beauchamp, C., Fridovich, I. 1971Superoxide dismutase: improved assays and an assay applicable to acrylamide gelsAnal. Biochem.44276CrossRefPubMedGoogle Scholar
  5. Blokhina, O., Virolainen, E., Fagerstedt, K. V. 2003Antioxidants, oxidative damage and oxygen deprivation stress: A reviewAnn. Bot.91179194CrossRefPubMedGoogle Scholar
  6. Borrell, A., Carbonell, L., Farras, R., Puig-Parellada, P., Tiburcio, A. F. 1997Polyamines inhibit lipid peroxidation in senescing oat leavesPhysiol. Plant.99385390CrossRefGoogle Scholar
  7. Bors, W., Langebartels, C., Michel, C., Sandermann, H.,Jr. 1989Polyamines as radical scavengers and protectants against ozone damagePhytochemistry2815891595CrossRefGoogle Scholar
  8. Bradford, M. M. 1976A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye bindingAnal. Biochem.72248254PubMedGoogle Scholar
  9. Bradford, K. J., Hsiao, T. C. 1982Physiological responses to moderate water stressLange, O. L.Nobel, P. S.Osmond, C. B.Ziegler, H. eds. Encyclopedia of Plant Physiology. New Ser. V 12 Sec. 2Springer-VerlagBerlin263324Google Scholar
  10. Burgos, N. R., Talbert, R. E., Kim, K. S., Kuk, Y. I. 2004Growth inhibition and root ultrastructure of cucumber seedlings exposed to allelochemicals from rye (Secale cereale)J. Chem. Ecol.30671689CrossRefPubMedGoogle Scholar
  11. Cameron, H. J., Julian, G. R. 1980Inhibition of protein synthesis in lettuce (Lactuca sativa) by allelopathic compoundsJ. Chem. Ecol.6989995CrossRefGoogle Scholar
  12. Chapin, F. S.,III, Shaver, G. R., Kedrowski, R. A. 1986Environmental controls over carbon, nitrogen, and phosphorus chemical fractions in Eriophorum vaginatum L. in Alaskan tussock tundraJ. Ecol.74167195Google Scholar
  13. Chiapusio, G., Sanchez, A. M., Reigosa, M. J., Gonzalez, L., Pellissier, F. 1997Do germination indices adequately reflect allelochemical effects on the germination process?J. Chem. Ecol.2324452453CrossRefGoogle Scholar
  14. Chifflet, S., Torriglia, A., Chiesa, R., Tolosa, S. 1988A method for the determination of inorganic phosphate in the presence of labile organic phosphate and high concentration of protein: Application to lens ATPasesAnal. Biochem.16814CrossRefPubMedGoogle Scholar
  15. Cruz-Ortega, R., Anaya, A. L., Gavilanes-Ruiz, M., Sanchez Nieto, S., Jimenez Estrada, M. 1990Effect of diacetyl piquerol on H+-ATPase activity of microsomes from Ipomoea purpureaJ. Chem. Ecol.1622532261CrossRefGoogle Scholar
  16. Davies, K. J. A. 1987Protein damage and degradation by oxygen radicalsJ. Biol. Chem.26298959901PubMedGoogle Scholar
  17. Dayan, F. E., Romagni, J. G., Tellez, M., Rimando, A., Duke, S. 1999Managing weeds with natural productsPestic. Outlook5185188Google Scholar
  18. Dhindsa, R. S., Plumb-Dhindsa, P., Thorpe, T. A. 1981Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalaseJ. Exp. Bot.3293101Google Scholar
  19. Einhellig, F. A. 1986Mechanisms and mode of action of allelochemicalsPutnam, A. R.Tang, C. S. eds. The Science of AllelopathyWileyNew York171188Google Scholar
  20. Epron, D., Dreyer, E., Breda, N. 1992Photosynthesis of oak trees [Quercus petraea (Matt.) Liebl.] during drought under field conditions: diurnal course of net CO2 assimilation and photochemical efficiency of photosystem IIPlant Cell Environ.15809820Google Scholar
  21. Frenkel, C. 1991Disruption of macromolecular hydration. A possible origin of chilling destabilisation of biopolymersTrends Food Sci. Technol.23941CrossRefGoogle Scholar
  22. Friebe, A., Roth, U., Kück, P., Schnabl, H., Schulz, M. 1997Effects of 2,4-dihydroxy-1,4-benzoxazin-3-ones on the activity of plasma membrane H+-ATPasePhytochemistry44979983CrossRefGoogle Scholar
  23. Genty, B., Brintais, J. M., Baker, N. R. 1989The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescenceBiochim. Biophys. Acta9908792Google Scholar
  24. Gonzalez, L. 2001Determination of water potential in leavesReigosa, M. J. eds. Handbook of Plant Ecophysiology TechniquesKluwer Academic PublishersDordrecht193206Google Scholar
  25. Heath, R. L., Packer, L. 1968Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidationArch. Biochem. Biophys.25189198CrossRefGoogle Scholar
  26. Hirt, H. 2000Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathwayProc. Natl. Acad. Sci.9724052407CrossRefPubMedGoogle Scholar
  27. Hoagland, D. R. and Arnon D. J. 1950. The water-culture method of growing plants without soil. Calif. Agric. Exp. Stn. 347.Google Scholar
  28. Jabs, T., Tschöpe, M., Colling, C. H., Hahlbrock, K., Scheel, D. 1997Elicitor-stimulated ion fluxes and O2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsleyProc. Natl. Acad. Sci. U.S.A.9448004805CrossRefPubMedGoogle Scholar
  29. Kao, C. H. 1997Physiological significance of stress-induced changes in polyamines in plantsBot. Bull. Acad. Sin.38141144Google Scholar
  30. Kilpeläinen, P. 2002. Ornithine decarboxylase. Expression and regulation in rat brain and in transgenic mice. PhD dissertation, Oulu University, Finland.Google Scholar
  31. Larcher, W. 1980Physiological Plant EcologySpringer-VerlagNew YorkGoogle Scholar
  32. Li, L., Li, J., Rao, J. N., Li, M., Bass, B. L., Wang, J. Y. 1999Inhibition of polyamine synthesis induces p53 gene expression but not apoptosisAm. J. Physiol.276C946C954PubMedGoogle Scholar
  33. Meister, H., Bolhàr-Nordenkampf, H. R. 2001Stomata imprints. A new and quick method to count stomata and epidermis cellsReigosa, M. J. eds. Handbook of Plant Ecophysiology TechniquesKluwer Academic PublishersDordrecht235250Google Scholar
  34. Niemeyer, H. M., Corcuera, L. J., Perez, F. J. 1982Reaction of a cyclic hydroxamic acid from Gramineae with thiolsPhytochemistry2122872289CrossRefGoogle Scholar
  35. Niemeyer, H. M., Calcaterra, N. B., Roveri, O. A. 1987Inhibition of energy metabolism by benzoxazolin-2-oneComp. Biochem. Physiol.873539Google Scholar
  36. Nilsen, E. T., Orcutt, D. M. 1996Physiology of Plants Under StressWileyNew YorkGoogle Scholar
  37. Nitta, T., Igarashi, K., Yamashita, A., Yamamoto, M., Yamamoto, N. 2001Involvement of polyamines in B cell receptor-mediated apoptosis: spermine functions as negative modulatorExp. Cell Res.265174183CrossRefPubMedGoogle Scholar
  38. Palmgren, M. G. 1998Proton gradients and plant growth: Role of the plasma membrane H+-ATPaseAdv. Bot. Res.28170Google Scholar
  39. Pedrol, N., Tiburcio, A. F. 2001Polyamines determination by TLC and HPLCReigosa, M. J. eds. Handbook of Plant Ecophysiology TechniquesKluwer Academic PublishersDordrecht335364Google Scholar
  40. Pedrol, N., Ramos, P., Reigosa, M. J. 2000Phenotypic plasticity and acclimation to water deficits in velvet-grass: A long-term greenhouse experiment. Changes in leaf morphology, photosynthesis and stress-induced metabolitesJ. Plant Physiol.157383393Google Scholar
  41. Perez, F. J. 1990Allelopathic effect of hydroxamic acids from cereals on Avena sativa and A. fatuaPhytochemistry29773776CrossRefGoogle Scholar
  42. Peters, W. P., Shpall, E. J., Jones, R. B., Olsen, G. A., Bast, R. C., Gockerman, J. P. 1988High dose combination alkylating agents with bone marrow support as an initial treatment for metastatic breast cancerJ. Clin. Oncol.613681376PubMedGoogle Scholar
  43. Prudencio-Ferreira, S. H., Areas, J. A. G. 1993Protein–protein interactions in the extrusion of soya at various temperatures and moisture contentsJ. Food Sci.58378381Google Scholar
  44. Ramos, P., Pedrol, N. 2001Free proline quantificationReigosa, M. J. eds. Handbook of Plant Ecophysiology TechniquesKluwer Academic PublishersDordrecht365382Google Scholar
  45. Reigosa, M. J., González, L. 2001Plant water statusReigosa, M. J. eds. Handbook of Plant Ecophysiology TechniquesKluwer Academic PublishersDordrecht185191Google Scholar
  46. Reigosa, M. J., Gonzalez, L., Sanchez-Moreiras, A. M., Duran, B., Puime, O., Fernandez, A., Bolaño, J. C. 2001Comparison of physiological effects of allelochemicals and commercial herbicidesAllelopathy J.8211220Google Scholar
  47. Sánchez-Moreiras, A. M., Weiss, O., Reigosa, M. J. 2004Allelopathic evidence in PoaceaeBot. Rev.69300319Google Scholar
  48. Schipper, R. G., Penning, L. C., Verhofstad, A. A. 2000Involvement of polyamines in apoptosis. Facts and controversies: effectors or protectors?Semin. Biol.105568CrossRefGoogle Scholar
  49. Silva, E., Nogueira, J. N. 1984Estudo da actividade da polifenol oxidase e da peroxidase em algumas frutas e hortaliçasO Solo764351Google Scholar
  50. Stoscheck, C. M. 1990Quantitation of proteinMethods Enzymol.1825069PubMedGoogle Scholar
  51. Virtanen, A. I., Hietala, P. K., Wahlross, O. 1957Antimicrobial substances in cereals and fodder plantsArch. Biochem. Biophys.69486500CrossRefPubMedGoogle Scholar
  52. Wen, J. Q., Tan, B. C., Liang, H. G. 1996Changes in protein and amino acid levels during growth and senescence of Nicotiana rustica callusJ. Plant Physiol.148707710Google Scholar
  53. Zeng, R. S., Luo, S. M., Shi, Y. H., Shi, M. B., Tu, C. Y. 2001Physiological and biochemical mechanism of allelopathy of secalonic acid F on higher plantsAgron. J.937279Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Laboratory of Plant Ecophysiology, Faculty of BiologyUniversity of VigoVigoSpain
  2. 2.Max-Planck-Institut für Chemische OkologieBeutenberg CampusJenaGermany

Personalised recommendations