Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-06-11T10:55:33.541Z Has data issue: false hasContentIssue false

Sequestration and Oxygen Radical Detoxification as Mechanisms of Paraquat Resistance

Published online by Cambridge University Press:  12 June 2017

Jonathan J. Hart
Affiliation:
Dep. Soil, Crop, and Atmos. Sci., Cornell Univ., Ithaca, NY 14853
Joseph M. Di Tomaso
Affiliation:
Dep. Soil, Crop, and Atmos. Sci., Cornell Univ., Ithaca, NY 14853

Abstract

Evidence in the literature has generally supported either of two paraquat resistance mechanisms: an increase in activity of oxygen radical-scavenging enzymes in resistant plants which affords protection from active oxygen species formed by paraquat; and sequestration of paraquat away from its site of action in the chloroplast. Evidence for the first model relies primarily on measurement of increased enzyme activity and cross-resistance to other oxygen radical-generating stresses in resistant plants. The sequestration model is supported by data showing decreased translocation of paraquat and absence of paraquat injury in plant systems that do not have increased levels of protective enzymes. An alteration in paraquat transport at one of several plant cell membranes could confer resistance by modifying movement of paraquat into the compartment bounded by that membrane. Properties of the plasmalemma, chloroplast envelope, and tonoplast that may be important to paraquat transport are discussed and data supporting or discounting specific membrane alterations in resistant plants are presented. Finally, the possibility that both mechanisms may work in concert is addressed.

Type
Special Topics
Copyright
Copyright © 1994 by the Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

1. Bagni, N. and Pistocchi, R. 1985. Putrescine uptake in Saintpaulia petals. Plant Physiol. 77:398402.CrossRefGoogle ScholarPubMed
2. Bishop, T., Powles, S. B., and Cornic, G. 1987. Mechanism of paraquat resistance in Hordeum glaucum. II. Paraquat uptake and translocation. Aust. J. Plant Physiol. 14:539547.Google Scholar
3. Blumwald, E. 1987. Tonoplast vesicles as a tool in the study of ion transport at the plant vacuole. Physiol. Plant. 69:731734.CrossRefGoogle Scholar
4. Cakmak, I. and Marschner, H. 1992. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 98:12221227.CrossRefGoogle ScholarPubMed
5. Cakmak, I. and Marschner, H. 1992. Magnesium deficiency enhances resistance to paraquat toxicity in bean leaves. Plant Cell Environ. 15:955960.CrossRefGoogle Scholar
6. Calderbank, A. 1968. The bipyridylium herbicides. Adv. Pest Cont. Res. 8:127235.Google ScholarPubMed
7. Carroll, E. W., Schwarz, O. J., and Hickock, L. G. 1988. Biochemical studies of paraquat-tolerant mutants of the fern Ceratopteris richardii . Plant Physiol. 87:651654.CrossRefGoogle ScholarPubMed
8. Carroll, A. D., Stewart, G. R., and Phillips, R. 1992. Dynamics of nitrogenous assimilate partitioning between cytoplasmic and vacuolar fractions in carrot cell suspension cultures. Plant Physiol. 100:18081814.CrossRefGoogle ScholarPubMed
9. Dainty, J., Hope, A. B., and Denby, C. 1960. Ionic relations of cells of Chara australis. II. The indiffusible anions of the cell wall. Aust. J. Biol. Sci. 13:267276.CrossRefGoogle Scholar
10. Demming, B. and Gimmler, H. 1983. Properties of the isolated intact chloroplast at cytoplasmic K+ concentrations. I. Light-induced cation uptake into intact chloroplasts is driven by an electrical potential difference. Plant Physiol. 73:169174.CrossRefGoogle Scholar
11. Dietz, K., Jäger, R., Kaiser, G., and Martinoia, E. 1990. Amino acid transport across the tonoplast of vacuoles isolated from barley mesophyll protoplasts. Plant Physiol. 92:123129.CrossRefGoogle ScholarPubMed
12. DiTomaso, J. M., Hart, J. J., and Kochian, L. V. 1993. Compartmentation analysis of paraquat fluxes in maize roots as a means of estimating the rate of vacuolar accumulation and translocation to shoots. Plant Physiol. 102:467472.CrossRefGoogle ScholarPubMed
13. DiTomaso, J. M., Hart, J. J., Linscott, D. L., and Kochian, L. V. 1992. Effect of inorganic cations and metabolic inhibitors on putrescine transport in roots of intact maize seedlings. Plant Physiol. 99:508514.CrossRefGoogle ScholarPubMed
14. Dodge, J. D. and Lawes, G. B. 1974. Some effects of the herbicides diquat and morfamquat on the fine structure of leaf cells. Weed Res. 14:4549.CrossRefGoogle Scholar
15. Fuerst, E. P., Nakatani, H. Y. Dodge, A. D., Penner, D., and Arntzen, C. J. 1985. Paraquat resistance in Conyza . Plant Physiol. 77:984989.CrossRefGoogle ScholarPubMed
16. Fuerst, E. P. and Vaughn, K. C. 1990. Mechanisms of paraquat resistance Weed Technol. 4:150156.CrossRefGoogle Scholar
17. Funderburk, H. H. Jr. and Bozarth, G. A. 1967. Review of the metabolism and decomposition of diquat and paraquat. J. Agric. Food Chem. 15:563567.CrossRefGoogle Scholar
18. Furasawa, I., Tanaka, K., Thanutong, P., Mizuguchi, A., Yazaki, M., and Asada, K. 1984. Paraquat resistant tobacco calluses with enhanced superoxide dismutase activity. Plant Cell Physiol. 25:12471254.Google Scholar
19. Harper, D. B. and Harvey, B. M. R. 1978. Mechanism of paraquat tolerance in perennial ryegrass. II. Role of superoxide dismutase, catalase and peroxidase. Plant Cell Environ. 1:211215.CrossRefGoogle Scholar
20. Hart, J. J. and DiTomaso, J. M. 1994. Paraquat transport in plasmalemma vesicles from leaves of paraquat-resistant and -susceptible wall barley (Hordeum glaucum Steud.). Weed Sci. Soc. Am. Abstr. 34:58.Google Scholar
21. Hart, J. J., DiTomaso, J. M., Linscott, D. L., and Kochian, L. V. 1992. Characterization of the transport and cellular compartmentation of paraquat in roots of intact maize seedlings. Pestic. Biochem. Physiol. 43:212222.CrossRefGoogle Scholar
22. Hart, J. J., DiTomaso, J. M., Linscott, D. L., and Kochian, L. V. 1992. Transport interactions between paraquat and polyamines in roots of intact maize seedlings. Plant Physiol. 99:14001405.CrossRefGoogle ScholarPubMed
23. Hart, J. J., DiTomaso, J. M., Linscott, D. L., and Kochian, L. V. 1993. Investigations into the cation specificity and metabolic requirements for paraquat transport in roots of intact maize seedlings. Pestic. Biochem. Physiol. 45:6271.CrossRefGoogle Scholar
24. Harvey, B. M. R., Muldoon, J., and Harper, D. B. 1978. Mechanism of paraquat tolerance in perennial ryegrass. I. Uptake, metabolism and translocation of paraquat. Plant Cell Environ,. 1:203209.CrossRefGoogle Scholar
25. Heber, U. and Heldt, H. W. 1981. The chloroplast envelope: structure, function and role in leaf metabolism. Annu. Rev. Plant Physiol. 32:139168.CrossRefGoogle Scholar
26. Heldt, H. W. and Flügge, U. I. 1987. Subcellular transport of metabolites in plant cells. Pages 4985 in Davies, D. D., ed. The Biochemistry of Plants. Vol. 12. Academic Press, San Diego.Google Scholar
27. Iwasaki, I., Arata, H., Kijima, H., and Nishimura, M. 1992. Two types of channels involved in the malate ion transport across the tonoplast of a crassulacean acid metabolism plant. Plant Physiol. 98:14941497.CrossRefGoogle ScholarPubMed
28. Jansen, M. A. K., Malan, C., Shaaltiel, Y., and Gressel, J. 1990. Mode of evolved photooxidant resistance to herbicides and xenobiotics. Z. Naturforsch. 45c:463469.CrossRefGoogle Scholar
29. Jansen, M. A. K., Shaaltiel, Y., Kazzes, D., Canaani, O., Malkin, S., and Gressel, J. 1989. Increased tolerance to photoinhibitory light in paraquat-resistant Conyza bonariensis measured by photoacoustic spectroscopy and 14CO2-fixation. Plant Physiol. 91:11741178.CrossRefGoogle Scholar
30. Kao, S. M. and Hassan, H. M. 1985. Biochemical characterization of a paraquat-tolerant mutant of Escherichia coli . J. Biol. Chem. 260:1047810481.CrossRefGoogle ScholarPubMed
31. Kochian, L. V., Shaff, J. E., and Lucas, W. J. 1989. High affinity K+ uptake in maize roots. Plant Physiol. 91:12021211.CrossRefGoogle ScholarPubMed
32. Kyle, D. J. 1987. The biochemical basis for photoinhibition of photosystem II. Pages 197226 in Kyle, D. J., Osmond, C. B., and Arntzen, C. J., eds. Photoinhibition, Topics in Photosynthesis. Vol. 9. Elsevier, Amsterdam.Google Scholar
33. Lehoczki, E., Laskay, G., Gaál, I., and Szigeti, Z. 1992. Mode of action of paraquat in leaves of paraquat-resistant Conyza canadensis (L.) Cronq. Plant Cell Environ. 15:531539.CrossRefGoogle Scholar
34. Morimyo, M., Hongo, E., Hama-Inaba, H., and Machida, I. 1992. Cloning and characterization of the mvrC gene of Escherichia coli K-12 which confers resistance against methyl viologen toxicity. Nucleic Acids Res. 20:31593165.CrossRefGoogle ScholarPubMed
35. Pistocchi, R., Keller, F., Bagni, N., and Matile, P. 1988. Transport and subcellular localization of polyamines in carrot protoplasts and vacuoles. Plant Physiol. 87:514518.CrossRefGoogle ScholarPubMed
36. Polos, E., Mikulás, J., Szigeti, Z., Matkovics, B., Hai, D. Q., Párducz, Á., and Lehoczki, E. Paraquat and atrazine co-resistance in Conyza canadensis (L.) Cronq. Pestic. Biochem. Physiol. 30:142154.CrossRefGoogle Scholar
37. Powles, S. B. 1986. Appearance of a biotype of the weed, Hordeum glaucum Steud., resistant to the herbicide paraquat. Weed Res. 26:167172.CrossRefGoogle Scholar
38. Powles, S. B. and Cornic, G. 1987. Mechanism of paraquat resistance in Hordeum glaucum. I. Studies with isolated organelles and enzymes. Aust. J. Plant Physiol. 14:8189.Google Scholar
39. Preston, C., Holtum, J. A. M., and Powles, S. B. 1992. Do polyamines contribute to paraquat resistance in Hordeum glaucum Pages 571574 in Murata, N., ed. Research in Photosynthesis. Vol. 3. Kluwer Academic Publishers, Netherlands.CrossRefGoogle Scholar
40. Preston, C., Holtum, J. A. M., and Powles, S. B. 1992. On the mechanism of resistance to paraquat in Hordeum glaucum and H. leporinum . Plant Physiol. 100:630636.CrossRefGoogle ScholarPubMed
41. Preston, C., Holtum, J. A. M., and Powles, S. B. 1991. Resistance to the herbicide paraquat and increased tolerance to photoinhibition are not correlated in several weed species. Plant Physiol. 96:314318.CrossRefGoogle Scholar
42. Purba, E., Preston, C., and Powles, S. B. 1992. Temperature influence on the level of resistance to paraquat in a biotype of Hordeum leporinum Link. Proc. Int. Weed Control Conf. 1:911.Google Scholar
43. Ranade, S. and Feierabend, J. 1991. Comparison of light-induced stress reactions in susceptible and paraquat-tolerant green cell cultures of Chenopodium rubrum L. J. Plant Physiol. 137:749752.CrossRefGoogle Scholar
44. Rona, J., Pitman, M. G., Lüttge, U., and Ball, E. 1980. Electrochemical data on compartmentation into cell wall, cytoplasm, and vacuole of leaf cells in the CAM genus Kalanchoë . J. Membr. Biol. 57:2535.CrossRefGoogle Scholar
45. Shaaltiel, Y., Chua, N.-H., Gepstein, S., and Gressel, J. 1988. Dominant pleiotropy controls enzymes co-segregating with paraquat resistance in Conyza bonariensis . Theor. Appl. Genet. 75:850856.CrossRefGoogle Scholar
46. Shaaltiel, Y., Glazer, A., Bocion, P. F., and Gressel, J. 1988. Cross tolerance to herbicidal and environmental oxidants of plant biotypes tolerant to paraquat, sulfur dioxide and ozone. Pestic. Biochem. Physiol. 31:1323.CrossRefGoogle Scholar
47. Shaaltiel, Y. and Gressel, J. 1987. Kinetic analysis of resistance to paraquat in Conyza . Plant Physiol. 85:869871.CrossRefGoogle ScholarPubMed
48. Shaaltiel, Y. and Gressel, J. 1986. Multienzyme oxygen radical detoxifying system correlated with paraquat resistance in Conyza bonariensis . Pestic. Biochem. Physiol. 26:2228.CrossRefGoogle Scholar
49. Slade, P. 1966. The fate of paraquat applied to plants. Weed Res. 6:158167.CrossRefGoogle Scholar
50. Spanswick, R. M. 1970. Electrophysiological techniques and the magnitude of the membrane potentials and resistances of Nitella translucens . J. Exp. Bot. 21:617627.CrossRefGoogle Scholar
51. Tanaka, K., Furusawa, I., Kondo, N., and Tanaka, K. 1988. SO2 tolerance of tobacco plants regenerated from paraquat-tolerant callus. Plant Cell Physiol. 29:743746.Google Scholar
52. Tanaka, Y., Chisaka, H., and Saka, H. 1986. Movement of paraquat in resistant and susceptible biotypes of Erigeron philadelphicus and E. canadensis . Physiol. Plant. 66:605608.CrossRefGoogle Scholar
53. Weibe, H. H. 1978. The significance of plant vacuoles. Bioscience 28:327331.CrossRefGoogle Scholar
54. Wu, W., Peters, J., and Berkowitz, G. A. 1991. Surface charge-mediated effects of Mg2+ on K+ flux across the chloroplast envelope are associated with regulation of stromal pH and photosynthesis. Plant Physiol. 97:580587.CrossRefGoogle Scholar
55. Vaughn, K. C. and Fuerst, E. P. 1985. Structural and physiological studies of paraquat-resistant Conyza . Pestic. Biochem. Physiol. 24:8694.CrossRefGoogle Scholar
56. Vaughn, K. C., Vaughn, M. A., and Camilleri, P. 1989. Lack of cross-resistance of paraquat-resistant hairy fleabane (Conyza bonariensis) to other toxic oxygen generators indicates enzymatic protection is not the resistant mechanism. Weed Sci. 37:511.CrossRefGoogle Scholar
57. Youngman, R. J. and Dodge, A. D. 1981. On the mechanism of paraquat resistance in Conyza sp. Pages 537544 in Akoyunoglou, G., ed. Photosynthesis and Plant Productivity, Photosynthesis and Environment. Balaban, Philadelphia.Google Scholar