Skip to main content
SpringerLink
Log in

Changes in the binding and inhibitory properties of urea/triazine-type herbicides upon phospholipid and galactolipid depletion in the outer monolayer of thylakoid membranes

Different behaviour of atrazine-susceptible and-resistant biotypes of Solanum nigrum L.

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The binding characteristics and the inhibitory power of atrazine and DCMU towards uncoupled electron flow activity were studied in acyl lipid-depleted thylakoid membranes from atrazine-susceptible and-resistant biotypes of Solanum nigrum L. For this purpose, phospholipase A2 from Vipera russelli and the lipase from Rhizopus arrhizus were used to obtain a selective lipid class (phospholipids or galactolipids) depletion which was restricted to the outer monolayer. Neither phospholipid nor galactolipid removal affected the dissociation constant and the number of binding sites of atrazine. In contrast, the dissociation constant of DCMU was increased in phospholipid-depleted thylakoid membranes but remained unchanged after galactolipid depletion. The number of DCMU binding sites decreased significantly after both lipase treatments, but only in the resistant biotype. The inhibitory effectiveness of the herbicide was either decreased or increased (to different extents) depending on the lipid class which was removed from the membrane and on the biotype considered. These results are discussed with reference to the possible conformational changes of the 32 kDa herbicide-binding polypeptide occurring after lipase treatments.

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

Abbreviations

Atrazine:

2-chloro-4-(ethylamino)-6-(isopropylamino)-s-triazine

BSA:

bovine serum albumin

DCMU:

diuron, 3-(3,4-dichlorophenyl)-1,1-dimethylurea

DGDG:

digalactosyldiacylglycerol

LRa:

lipase from Rhizopus arrhizus

MGDG:

monogalactosyldiacylglycerol

PC:

phosphatidylcholine

PG:

phosphatidylglycerol

PLA2 :

phospholipase A2

R:

atrazine-resistant

S:

atrazinesusceptible

References

  • Adir N and Ohad I (1986) Probing for the interaction of the 32 kDa-QB protein with its environment by use of bifunctional cross-linking reagents. Biochim Biophys Acta 850: 264–274

    Google Scholar 

  • Bruinsma J (1961) A comment on the spectrophotometric determination of chlorophyll. Biochim Biophys Acta 53: 576–587

    Google Scholar 

  • Burke JJ, Wilson F and Swafford JR (1982) Characterization of chloroplasts isolated from triazine-susceptible and triazine-resistant biotypes of Brassica campestris L. Plant Physiol 70: 24–29

    Google Scholar 

  • Fersht A (1977) Enzyme Structure and Mechanism, pp 1–371. WH Freeman and Company, Reading and San Francisco

    Google Scholar 

  • Gardner G (1989) A stereochemical model for the active site of Photosystem II herbicides. Photochem Photobiol 49: 331–336

    Google Scholar 

  • Giardi MT, Marder JB and Barber J (1988) Herbicide binding to the isolated Photosystem II reaction centre. Biochim Biophys Acta 934: 64–71

    Google Scholar 

  • Gounaris K and Barber J (1985) Isolation and characterization of a Photosystem II reaction center lipoprotein complex. FEBS Lett 188: 68–72

    Google Scholar 

  • Herrmann G, Thiel A and Böger P (1984) Herbicide-binding protein, binding sites and electron-transport activity: quantitative relations. Z Naturforsch 39c: 430–433

    Google Scholar 

  • Hirschberg J, Bleecker A, Kyle DJ, McIntosh L and Arntzen CJ (1984) The molecular basis of triazine-herbicide resistance in higher-plant chloroplasts. Z Naturforsch 39c: 412–420

    Google Scholar 

  • Horvath G, Droppa M and Melis A (1984) Herbicide action on Photosystem II in spinach chloroplasts: concentration effect on PS IIα and PS IIβ. Photobiochem Photobiophys 7: 249–256

    Google Scholar 

  • Horvath G, Melis A, Hideg E, Droppa M and Vigh L (1987) Role of lipids in the organiation and function of Photosystem II studied by homogeneous catalytic hydrogenation of thylakoid membranes in situ. Biochim Biophys Acta 891: 68–74

    Google Scholar 

  • Jursinic P and Denenberg R (1989) Measurement of stoichiometry of Photosystem II to Photosystem I reaction centers. Photosynth Res 21: 197–200

    Google Scholar 

  • Jursinic P and Stemler A (1983) Changes in [14C]Atrazine binding associated with the oxidation-reduction state of the secondary quinone acceptor of Photosystem II. Plant Physiol 73: 703–708

    Google Scholar 

  • Krupa Z (1983) The action of lipase on chloroplast membranes. II. Polypeptide patterns of bean galactolipase-and phospholipase A2-treated thylakoid membranes. Photosynth Res 4: 229–239

    Google Scholar 

  • Laasch H, Pfister K and Urbach W (1981) Comparative binding of Photosystem II-herbicides to isolated thylakoid membranes and intact green algae. Z Naturforsch 36c: 1041–1049

    Google Scholar 

  • Laasch H, Pfister K and Urbach W (1982) High-and low-affinity binding of Photosystem II herbicides to isolated thylakoid membranes and intact algal cells. Z Naturforsch 37c: 620–631

    Google Scholar 

  • Laasch H, Schreiber U and Urbach W (1984) Binding of radioactively labelled DCMU in dependence of the redox state of the Photosystem II acceptor side. In: Sybesma C (ed) Advances in Photosynthesis Research, Vol IV, pp 25–28. Nifhoff, M./Dr Junk, W. publishers, The Hague, Netherlands

    Google Scholar 

  • Lehoczki E, Pölös E, Laskay G and Farkas T (1985) Chemical compositions and physical states of chloroplast lipids related to atrazine resistance in Conyza canadensis L. Plant Science 42: 19–24

    Google Scholar 

  • Li G, Knowles PF, Murphy DJ, Nishida I and Marsh D (1989) Spin-label ESR studies of lipid-protein interactions in thylakoid membranes. Biochem 28: 7446–7452

    Google Scholar 

  • Millner PA, Grouzis JP, Chapman DJ and Barber J (1983) Lipid enrichment of thylakoid membranes. Biochim Biophys Acta 722: 331–340

    Google Scholar 

  • Neumann W, Laasch H and Urbach W (1984) Increased binding of [14C]ioxynil in unicellular green algae under anaerobiosis and by addition of other phenolic herbicides or uncouplers. Z Naturforsch 39c: 402–404

    Google Scholar 

  • Neumann W, Laasch H and Urbach W (1987) Mechanisms of herbicide sorption in microalgae and the influence of environmental factors. Pest Biochem Physiol 27: 189–200

    Google Scholar 

  • Oettmeier W, Kude C and Soll HJ (1987) Phenolic herbicides and their methylethers: binding characteristics and inhibition of photosynthetic electron transport and photophosphorylation. Pest Biochem Physiol 27: 50–60

    Google Scholar 

  • Oettmeier W, Masson K and Johanningmeier U (1982b) Evidence for two different herbicide-binding proteins at the reducing side of Photosystem II. Biochim Biophys Acta 679: 376–383

    Google Scholar 

  • Oettmeier W, Masson K, Fedtke C, Konze J and Schmidt RR (1982a) Effect of different Photosystem II inhibitors on chloroplasts isolated from species either susceptible or resistant toward s-triazine herbicides. Pest Biochem Physiol 18: 357–367

    Google Scholar 

  • Paterson, DR and Arntzen, CJ (1982) Detection of altered inhibition of Photosystem II reactions in herbicide-resistant plants. In: Edelman, et al. (eds) Methods in Chloroplast Molecular Biology, pp 109–118. Biomedical Press, Elsevier

  • Pfister K and Urbach N (1983) Effects of biocides and growth regulators: Physiological basis. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology IV, Encyclopedia of Plant Physiology, New Series, Vol 12D, pp 329–391. Springer, Berlin

    Google Scholar 

  • Pfister K, Radosevich SR and Arntzen CJ (1979) Modification of herbicide binding to Photosystem II in two biotypes of Senecio vulgaris L. Plant Physiol 64: 995–999

    Google Scholar 

  • Pillai P and St. John JB (1981) Lipid composition of chloroplast membranes from weed biotypes differentially sensitive to triazine herbicides. Plant Physiol 68: 585–587

    Google Scholar 

  • Rawyler A and Siegenthaler PA (1985) Transversal localization of monogalactosyldiacylglycerol and digalactosyldia-cylglycerol in spinach thylakoid membranes. Biochim Biophys Acta 815: 287–298

    Google Scholar 

  • Rawyler A, Unitt MD, Giroud C, Davies H, Mayor JP, Harwood JL and Siegenthaler PA (1987) The transmembrane distribution of galactolipids in chloroplast thylakoids is universal in a wide variety of temperate climate plants. Photosynth Res 11: 3–13

    Google Scholar 

  • Renger G, Hagemann R and Vermaas WFJ (1984) Studies on the functional mechanism of system II herbicides in isolated chloroplasts. Z Naturforsch 39c: 362–367

    Google Scholar 

  • Rivera CM and Penner D (1979) Effect of herbicides on plant cell membrane lipids. Residue Rev 70: 45–76

    Google Scholar 

  • Siegenthaler PA and Giroud C (1986) Transversal distribution of phospholipids in prothylakoid and thylakoid membranes from oat. FEBS Lett 201: 215–220

    Google Scholar 

  • Siegenthaler PA, Rawyler A and Smutny J (1989) The phospholipid population which sustains the uncoupled noncyclic electron flow activity is localized in the inner monolayer of the thylakoid membrane. Biochim Biophys Acta 975: 104–111

    Google Scholar 

  • Siegenthaler PA, Smutny J and Rawyler A (1987) Involvement of distinct populations of phosphatidylglycerol and phosphatidylcholine molecules in photosynthetic electronflow activities. Biochim Biophys Acta 891: 85–93

    Google Scholar 

  • Siegenthaler PA, Sutter J and Rawyler A (1988) The transmembrane distribution of galactolipids in spinach thylakoid inside-out vesicles is opposite to that found in intact thylakoids. FEBS Lett 228: 94–98

    Google Scholar 

  • Sigematsu Y, Sato F and Yamada Y (1989) The mechanism of herbicide resistance in tobacco cells with a new mutation in the QB protein. Plant Physiol 89: 986–992

    Google Scholar 

  • Sinning I, Koepke J and Michel H (1990) Recent advances in the structure analysis of Rhodopseudomonas viridis reaction center mutants. In: Michel H and Beyerle H (eds) Reaction Centres of Photosynthetic Bacteria, Springer Series in Biophysics, Vol 6, pp 199–209. Springer Verlag

  • Soll HJ and Oettmeier W (1984) Inhibitor binding and displacement in plastoquinone depleted chloroplasts. In: Sybesma C (ed) Advances in Photosynth Res, Vol IV, pp 5–8. The Hague, Nijhoff, M./Dr Junk, W. Publishers, The Netherlands

    Google Scholar 

  • Thiel A and Böger P (1984) Comparative herbicide binding by photosynthetic membranes from resistant mutants. Pest Biochem Physiol 22: 232–242

    Google Scholar 

  • Thomas PG, Brain APR, Quinn PJ and Williams WP (1985) Low pH and phospholipase A2 treatment induce the phaseseparation of non-bilayer lipids within pea chloroplast membranes. FEBS Lett 183: 161–166

    Google Scholar 

  • Tischer W and Strotmann H (1977) Relationship between inhibitor binding by chloroplasts and inhibition of photosynthetic electron transport. Biochim Biophys Acta 460: 113–125

    Google Scholar 

  • Trebst A (1987) The three-dimensional structure of the herbicide binding niche on the reaction center polypeptides of Photosystem II. Z Naturforsch 42c: 742–750

    Google Scholar 

  • Unitt MD and Harwood JL (1985) Sidedness studies of thylakoid phosphatidylglycerol in higher plants. Biochem J 228: 707–711

    Google Scholar 

  • Urbach W, Laasch H and Schreiber U (1984) Redox-state dependent changes of inhibitor-binding to the Photosystem II acceptor complex. Z Naturforsch 39c: 397–401

    Google Scholar 

  • Van Rensen JJS (1984) Interaction of Photosystem II herbicides with bicarbonate and formate in their effects on photosynthetic electron flow. Z. Naturforsch 39c: 374–377

    Google Scholar 

  • Vasil'ev IR, Matorin DN, Lyadsky VV and Venediktov PS (1988) Multiple action sites for Photosystem II herbicides as revealed by delayed fluorescence. Photosynth Res 15: 33–39

    Google Scholar 

  • Vermaas WFJ, Arntzen CJ, Gu LQ and Yu CA (1983) Interactions of herbicides and azidoquinones at a Photosystem II binding site in the thylakoid membrane. Biochim Biophys Acta 723: 266–275

    Google Scholar 

  • Vermaas WFJ, Kenger G and Arntzen CJ (1984) Herbicide/quinone binding interactions in Photosystem II. Z Naturforsch 39c: 368–373

    Google Scholar 

  • Wettern M (1986) Localization of 32 000 dalton chloroplast protein pools in thylakoids: significance in atrazine binding. Plant Science 43: 173–177

    Google Scholar 

  • Zierler K (1989) Misuse of nonlinear Scatchard plots. TIBs 14: 314–317

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Physiologie végétale, Université de Neuchâtel, 20, chemin de Chantermerle, CH-2000, Neuchâtel, Switzerland

    P. -A. Siegenthaler & J. -P. Mayor

Authors
  1. P. -A. Siegenthaler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. -P. Mayor
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siegenthaler, P.A., Mayor, J.P. Changes in the binding and inhibitory properties of urea/triazine-type herbicides upon phospholipid and galactolipid depletion in the outer monolayer of thylakoid membranes. Photosynth Res 31, 57–68 (1992). https://doi.org/10.1007/BF00049537

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00049537

Key words

Search

Navigation