Biologia plantarum 64: 335-342, 2020 | DOI: 10.32615/bp.2019.150

Imazamox detoxification and recovery of plants after application of imazamox to an imidazolinone resistant sunflower hybrid

D. BALABANOVA1,2,*, T. REMANS2, A. CUYPERS2, J. VANGRONSVELD2, A. VASSILEV1
1 Department of Plant Physiology and Biochemistry, Agricultural University of Plovdiv, BG-4000 Plovdiv, Bulgaria
2 Centre for Environmental Sciences, Hasselt University, BE-3590 Diepenbeek, Belgium

Imidazolinone herbicides combined with imidazolinone resistant (IMI-R) crops provide a tool for solving the important problem of the occurrence of weeds during the early growth stages of sunflower. These herbicides inhibit the synthesis of branched chain amino acids by interrupting the key enzyme acetohydroxyacid synthase (AHAS). We studied the imazamox detoxification in an IMI-R sunflower hybrid together with plant growth and photosynthetic performance. Inhibition of photosynthesis and growth were observed as initial effects of imazamox application. A slight decrease in AHAS activity was also noticed. These effects disappeared within two weeks after application. A fast and well-functioning detoxification mechanism for the herbicide, of which the content decreased for about 90 % at 14 d after application, seems to be responsible for this. The activity of the xenobiotic detoxifying enzyme glutathione S-transferases (GSTs) significantly increased after imazamox application. Our results suggest that the metabolite glutathione serves as an auxiliary tool for imazamox detoxification through conjugation reactions realized by the GSTs, thereby taking part in the non-target mechanisms of resistance in IMI-R sunflower hybrids.

Keywords: acetohydroxyacid synthase, chlorophyll, glutathione S-transferase, Helianthus annuus, photosynthesis.

Received: March 4, 2019; Revised: November 8, 2019; Accepted: December 2, 2019; Published online: April 24, 2020Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
BALABANOVA, D., REMANS, T., CUYPERS, A., VANGRONSVELD, J., & VASSILEV, A. (2020). Imazamox detoxification and recovery of plants after application of imazamox to an imidazolinone resistant sunflower hybrid. Biologia plantarum64, 335-342. doi: 10.32615/bp.2019.150.
Download citation

Supplementary files

Download fileBalabanova6198 Suppl.pdf

File size: 138.62 kB

References

  1. Anastasov, H.: Influence of imazamox on some anatomic indices in the leaves of sunflower plant (Helianthus annuus L.). - Gen. appl. Plant Physiol. 36: 64-68, 2010.
  2. Balabanova, D.A., Paunov, M., Goltsev, V., Cuypers, A., Vangronsveld, J., Vassilev, A.: Photosynthetic performance of the imidazolinone resistant sunflower exposed to single and combined treatment by the herbicide imazamox and an amino acid extract. - Front Plant Sci. doi: 10.3389/fpls.2016.01559, 2016. Go to original source...
  3. Balabanova, D., Remans, T., Vassilev, A., Cuypers, A., Vangronsveld, J.: Possible involvement of glutathione S-transferases in imazamox detoxification in an imidazolinone-resistant sunflower hybrid. - J. Plant Physiol. 221: 62-65, 2018. Go to original source...
  4. Balabanova, D. Vassilev, A.: Response of sunflower Clearfield hybrids to both recommendable and higher doses of imazamox herbicide - Agr. Sci. 8: 18:41-46, 2015.
  5. Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye-binding. - Anal Biochem 72: 248-254, 1976. Go to original source...
  6. Brown, M.A., Chiu, T.Y.: Miller P.: Hydrolytic Activation versus oxidative degradation of Assert herbicide, an imidazolinone aryl-carboxylate, in susceptible wild oat versus tolerant corn and wheat. - Pestic. Biochem. Physiol. 27: 24-29, 1987. Go to original source...
  7. Bukun, B., Nissen, S.J., Shaner, D.L., Vassos, J.D.: Imazamox absorption, translocation, and metabolism in red lentil and dry bean. - Weed Sci. 60: 350-354, 2012. Go to original source...
  8. Bustin, S.A., Beaulieu, J., Huggett, J., Jaggi, R., Kibenge, F.S.B., Olsvik, P.A., Penning, L.C., Toegel, S.: Practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. - BMC Plant Biol. 11: 74, 2010. Go to original source...
  9. Coupland, D., Lutman, P. J. W.: Investigations into the movement of glyphosate from treated to adjacent untreated plants. - Ann. appl. Biol. 101: 315-321, 1982. Go to original source...
  10. Cobb, A., Reade, J.P.H.: Herbicides and Plant Physiology. - Wiley-Blackwell, Oxford 2010. Go to original source...
  11. Domínguez-Mendez, R., Alcántara-de la Cruz, R., Rojano-Delgado, A., Fernández-Moreno, P.T., Aponte R, De Prado, R.: Multiple mechanisms are involved in new imazamox-resistant varieties of durum and soft wheat. - Sci Rep. 7: 14839, 2017. Go to original source...
  12. Fernandez, P., Di Rienzo, J.A., Moschen, S., Dosio, G.A.A.: Aguirrezábal, L.A.N., Hopp, H.E., Paniego, N., Heinz, R.A.: Comparison of predictive methods and biological validation for qPCR reference genes in sunflower leaf senescence transcript analysis. - Plant Cell Rep. 30: 63-74, 2011. Go to original source...
  13. Foyer, C.H., Noctor, G.: Ascorbate and glutathione: the heart of the redox hub. - Plant Physiol. 155: 2-18, 2001. Go to original source...
  14. García-Garijo, A., Tejera, N.A., Lluch, C., Palma, F.: Metabolic responses in root nodules of Phaseolus vulgaris and Vicia sativa exposed to the imazamox herbicide. - Pest Biochem. Physiol. 111: 14-23, 2014. Go to original source...
  15. Gaston, S., Zabalza, A., González, E.M., Arrese-Igor, C., Aparicio-Tejo, P.M., Royuela, M.: Imazethapyr, an inhibitor of the branched-chain amino acid biosynthesis, induces aerobic fermentation in pea plants. - Physiol. Plant. 114: 524-532, 2002. Go to original source...
  16. Habig, W.H., Pabst, M.J., Jakoby, W.B.: Glutathione S-transferases. The first enzymatic step in mercapturic and acid formation. - J. biol, Chem 249: 7130-7713, 1974.
  17. Jimenez, F., Fernandez, P., Rojano-Delgado, A.M., Alcantara, R., De Prado, R.: Resistance to imazamox in Clearfield soft wheat (Triticum aestivum L.). - Crop Protect. 78: 15-19, 2015. Go to original source...
  18. Jozefczak, M., Remans, T., Vangronsveld, J., Cuypers, A.: Glutathione is a key player in metal-induced oxidative stress defences. - Int. J. mol. Sci. 13: 3145-3175, 2012. Go to original source...
  19. Kaspar, M., Grondona, M., León, A., Zambelli, A.: Selection of a sunflower line with multiple herbicide tolerance that is reversed by the P450 inhibitor malathion. - Weed Sci. 59: 232-237, 2011. Go to original source...
  20. Kudsk, P., Kristensen, J.L.: Effect of environmental factors on herbicide performance. - In: Combellack J.H., Levich K.J., Richardson R.G. (ed): First International Weed Control Congress. pp. 173-186. Weed Science Society of Victoria, Melbourne 1992.
  21. Lamoureux, G.L., Rusness, D.G.: Glutathione in the metabolism and detoxification of the xenobiotics in plants. - In: De Kok, L.J., Stulen, I., Rennenberg, H., Brunold, C., Rauser, W. (ed.): Sulfur Nutrition and Assimilation in Higher Plants. Pp. 221-237. SPB Academic Publishers, The Hague 1993.
  22. LaRossa, R.A., Schloss, J.V.: The sulfonylurea herbicide sulfometuron methyl is anextremelypotent and selective inhibitor of acetolacetate synthase in Salmonella typhimurium. - J. biol. Chem. 259: 8753-8757, 1984.
  23. Lichtenthaler, H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. - Methods Enzymol. 148: 350-382, 1987. Go to original source...
  24. Manabe, Y., Tinker, N., Clville, A., Miki, B.: CSR1, the sole target of imidazolinone herbicide in Arabidopsis thaliana. - Plant Cell Physiol. 9: 1340-1358, 2007. Go to original source...
  25. Marrs, K.: The functions and regulation of glutathione S-transferases in plants. - Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 127-158, 1996. Go to original source...
  26. Mithila, J., Hall, J.C., Johnson, W.G., Kelley, K.B., Riechers, D.E.: Evolution of resistance to auxinic herbicides: historical perspectives, mechanisms of resistance, and implications for broadleaf weed management in agronomic crops. - Weed Sci. 59: 445-457, 2011. Go to original source...
  27. Monchiero, M., Gullino, M.L., Pugliese, M., Spadaro, D., Garibald,i A.: Efficacy of different chemical and biological products in the control of Pseudomonas syringae pv. actinidiae on kiwifruit. - Australasian Plant Pathol. 44: 13-23, 2015.
  28. Ochogavia, A.C., Gil, M., Picardi, L., Nestares, G.: Precision phenotyping of imidazolinone-induced chlorosis in sunflower. - Breed. Sci. 64: 416-421, 2014. Go to original source...
  29. Pfenning, M., Palfay, G., Guillet, T. The CLEARFIELD® technology - a new broad-spectrum post-emergence weed control system for European sunflower growers. - J. Plant Dis. Prot. 21 (Special Issue): 649-653, 2008.
  30. Qian, H., Lu, T., Peng, X., Han, X., Fu, Z.: Enantioselective phytotoxicity of the herbicide Imazethapyr on the response of the antioxidant system and starch metabolism in Arabidopsis thaliana. - Plos ONE 6: e 19451, 2011. Go to original source...
  31. Quevel, G., Noctor, G.: A plate reader method for the measurement of NAD, NADP, glutathione and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. - Anal Biochem, 363: 58-69, 2007. Go to original source...
  32. Ray, T.: Site of action of chlorsulfuron: inhibition of valine and isoleucine biosynthesis in plants. - Plant Physiol. 75: 827-831, 1984. Go to original source...
  33. Rojano-Delgado, A.M., Priego-Capote, F., De Castro, M.D.L., De Prado, R.: Mechanism of imazamox resistance of the Clearfield® wheat cultivar for better weed control. - Agron. Sustain. Dev. 35: 639-648, 2015. Go to original source...
  34. Rost, T.L.: The comparative cell cycle and metabolic effects of chemical treatments on root tip meristems. Chlorsulfuron. J. Plant Growth Regul. 3: 51-63, 1984. Go to original source...
  35. Sala, C.A., Bulos, M., Altieri, E., Weston, B.: Response to imazapyr and dominance relationships of two imidazolinone-tolerant alleles at the Ahasl1 locus of sunflower. - Theor. appl. Genet. 124: 385-396, 2012. Go to original source...
  36. Scalla, R., Roulet, A.: Cloning and characterization of a glutathione S-transferase induced by a herbicide safener in barley (Hordeum vulgare). - Physiol. Plant. 116: 336-344, 2002. Go to original source...
  37. Schröder, P., Götzberger, C.: Partial purification and characterization of glutathione S-transferase from leaves of Juniperus communis, Larix decidua and Taxus baccata. - Appl. Bot. 71: 31-37, 1997.
  38. Shaner, D.L.: Physiological effects of the imidazolinone herbicides. - In: Shaner, D.L., O'Connor, S.L. (ed.): The Imidazolinone Herbicides. Pp. 129-137. CRC Press, Boca Raton 1991.
  39. Shaner, D.L.: Imidazolinone herbicides -. In: Plummer, D., Ragsdalr, N. (ed.): Encyclopedia of Agrochemicals. Pp. 769-784. John Wiley and Sons, Hoboke 2003.
  40. Shaner, D.L., Reider, M.L.: Physiological responses of com (Zea mays) to AC 243,997 in combination with valine, leucine and isoleucine. - Pest. Biochem. Physiol. 25: 248-257, 1986. Go to original source...
  41. Sousa, C., Pinti J.J.O., Martinazzo, E.G., Perboni, A.T., Farias, M.E., Bacarini,. M.A.: Chlorophyll a fluorescence in rice plants exposed of herbicides of group imidazolinone. - Planta Daninha 32: 141-150, 2013.
  42. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., Speleman, F.: Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. - Genome Biol. 3: 0034.1-0034.11, 2002. Go to original source...
  43. Vercampt, H., Koleva, L., Vassilev, A., Horemans, N., Biermans, G., Vangronsveld, J., Cuypers, A.: The functional role of the photosynthetic apparatus in the recovery of Brassica napus plants from preemergent metazachlor exposure. J. Plant Physiol. 196: 99-105, 2016. Go to original source...
  44. Yuan, J.S., Tranel, P.J., Stewart, N., Jr.: Non-target-site herbicide resistance: a family business. - Trends Plant Sci. 12: 6-13, 2006. Go to original source...
  45. Zabalza, A., Gaston, S., Orcaray, L., Royuela, M.: Carbohydrate accumulation in leaves of plants treated with the herbicides chlorsulfuron or IM is due to a decrease in sink strength. - J. Agr. Food Chem. 52: 7601-7606, 2004. Go to original source...