Evaluation of spectrophotometric and HPLC methods for shikimic acid determination in plants: Models in glyphosate-resistant and -susceptible crops

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 6, 2011, Pages 2202-2212

  Zelaya, Ian A ^a,c   Anderson, Jennifer A H ^a   Owen, Micheal D K ^a   Landes, Reid D ^b  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

Author keywords

Alicyclic hydroxy acid; chromophore half life (t1 2); EPSPS EC 2.5.1.19; Glycine max (L.) Merr; glyphosate efficacy; herbicide resistance; molar absorptivity; periodate derivatization; shikimate; vicinal diol; Zea mays L

Indexed keywords

EPSPS EC 2.5.1.19; GLYCINE MAX; GLYPHOSATES; HERBICIDE RESISTANCE; HYDROXY ACIDS; MOLAR ABSORPTIVITY; PERIODATE DERIVATIZATION; SHIKIMATES; VICINAL DIOL; ZEA MAYS L;

AMINO ACIDS; CARBOXYLIC ACIDS; CHROMATOGRAPHY; CHROMOPHORES; CROPS; EXTRACTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH PRESSURE LIQUID CHROMATOGRAPHY; HISTOLOGY; PLANT EXTRACTS; RATING; SPECTROPHOTOMETERS; SPECTROPHOTOMETRY; WEED CONTROL;

HERBICIDES;

DRUG DERIVATIVE; GLYCINE; GLYPHOSATE; HERBICIDE; PLANT EXTRACT; SHIKIMIC ACID;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CROP; DRUG EFFECT; ECONOMICS; EVALUATION; HERBICIDE RESISTANCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METHODOLOGY; SPECTROPHOTOMETRY;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CROPS, AGRICULTURAL; GLYCINE; HERBICIDE RESISTANCE; HERBICIDES; MODELS, BIOLOGICAL; PLANT EXTRACTS; SHIKIMIC ACID; SPECTROPHOTOMETRY;

GLYCINE MAX; ZEA MAYS;

EID: 79952756382     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf1043426     Document Type: Article

References (75)

1. Jaworski, E. G. Mode of action of N -phosphonomethyl glycine: inhibition of aromatic amino acid biosynthesis J. Agric. Food Chem. 1972, 20, 1195-1198
2. Duke, S. O.; Powles, S. B. Glyphosate-resistant crops and weeds: now and in the future AgBioForum 2009, 12, 346-357
3. Owen, M. D.; Zelaya, I. A. Herbicide-resistant crops and weed resistance to herbicides Pest Manag. Sci. 2005, 61, 301-311 (Pubitemid 40321462)
4. Heap, I. The international survey of herbicide resistant weeds; http://www.weedscience.com (accessed Nov 8, 2010).
5. Amrhein, N.; Deus, B.; Gehrke, P.; Steinrücken, H. C. The site of inhibition of the shikimate pathway by glyphosate: II. Interference of glyphosate with chorismate formation in vivo and in vitro Plant Physiol. 1980, 66, 830-834
6. Amrhein, N.; Holländer, H. Light promotes the production of shikimic acid in buckwheat Naturwissenschaften 1981, 68, 43
7. Herrmann, K. M. The shikimate pathway: early steps in the biosynthesis of aromatic compounds Plant Cell 1995, 7, 907-919
8. Singh, B. K.; Siehl, D. L.; Connelly, J. A. Shikimate pathway: why does it mean so much to so many? Oxf. Surv. Plant Mol. Cell. Biol. 1991, 7, 143-185
9. Weaver, L. M.; Herrmann, K. M. Dynamics of the shikimate pathway in plants Trends Plant Sci. 1997, 2, 346-351 (Pubitemid 27377995)
10. Herrmann, K. M.; Weaver, L. M. The shikimate pathway Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 473-503 (Pubitemid 129491971)
11. Lewis, J.; Johnson, K. A.; Anderson, K. S. The catalytic mechanism of EPSP synthase revisited Biochemistry 1999, 38, 7372-7379
12. Steinrücken, H. C.; Amrhein, N. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase Biochem. Biophys. Res. Commun. 1980, 94, 1207-1212 (Pubitemid 10016727)
13. Schönbrunn, E.; Eschenburg, S.; Shuttleworth, W. A.; Schloss, J. V.; Amrhein, N.; Evans, J. N. S.; Kabsch, W. Interaction of the herbicide glyphosate with its target enzyme 5-enolpyruvylshikimate 3-phosphate synthase in atomic detail Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 1376-1380 (Pubitemid 32165506)
14. Holländer-Czytko, H.; Amrhein, N. Subcellular compartmentation of shikimic acid and phenylalanine in buckwheat cell suspension cultures grown in the presence of shikimate pathway inhibitors Plant Sci. Lett. 1983, 29, 89-96
15. 13C NMR studies Biochimie 1992, 74, 875-882
16. Henry, W. B.; Shaner, D. L.; West, M. S. Shikimate accumulation in sunflower, wheat, and proso millet after glyphosate application Weed Sci. 2007, 55, 1-5 (Pubitemid 46213293)
17. Buehring, N. W.; Massey, J. H.; Reynolds, D. B. Shikimic acid accumulation in field-grown corn (Zea mays) following simulated glyphosate drift J. Agric. Food Chem. 2007, 55, 819-824
18. Reddy, K. N.; Ding, W.; Zablotowicz, R. M.; Thomson, S. J.; Huang, Y.; Krutz, L. J. Biological responses to glyphosate drift from aerial application in non-glyphosate-resistant corn Pest Manag. Sci. 2010, 66, 1148-1154
19. Singh, B. K.; Shaner, D. L. Rapid determination of glyphosate injury to plants and identification of glyphosate-resistant plants Weed Technol. 1998, 12, 527-530 (Pubitemid 28436984)
20. Harring, T.; Streibig, J. C.; Husted, S. Accumulation of shikimic acid: a technique for screening glyphosate efficacy J. Agric. Food Chem. 1998, 46, 4406-4412 (Pubitemid 128488551)
21. Bresnahan, G. A.; Manthey, F. A.; Howatt, K. A.; Chakraborty, M. Glyphosate applied preharvest induces shikimic acid accumulation in hard red spring wheat (Triticum aestivum) J. Agric. Food Chem. 2003, 51, 4004-4007
22. Mueller, T. C.; Massey, J. H.; Hayes, R. M.; Main, C. L.; Stewart, C. N. J. Shikimate accumulates in both glyphosate-sensitive and glyphosate-resistant horseweed (Conyza canadensis L. Cronq.) J. Agric. Food Chem. 2003, 51, 680-684
23. Zelaya, I. A.; Owen, M. D. K.; VanGessel, M. J. Inheritance of evolved glyphosate resistance in Conyza canadensis (L.) Cronq Theor. Appl. Genet. 2004, 110, 58-70 (Pubitemid 40240638)
24. Zelaya, I. A.; Owen, M. D. K. Differential response of Amaranthus tuberculatus (Moq ex DC) JD Sauer to glyphosate Pest Manag. Sci. 2005, 61, 936-950 (Pubitemid 41367959)
25. Zelaya, I. A.; Owen, M. D. K.; VanGessel, M. J. Transfer of glyphosate resistance: evidence of hybridization in Conyza (Asteraceae) Am. J. Bot. 2007, 94, 660-673 (Pubitemid 46955006)
26. Gaines, T. A.; Zhang, W.; Wang, D.; Bukun, B.; Chisholm, S. T.; Shaner, D. L.; Nissen, S. J.; Patzoldt, W. L.; Tranel, P. J.; Culpepper, A. S.; Grey, T. L.; Webster, T. M.; Vencill, W. K.; Sammons, R. D.; Jiang, J.; Preston, C.; Leach, J. E.; Westra, P. Gene amplification confers glyphosate resistance in Amaranthus palmeri Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 1029-1034
27. Mossor-Pietraszewska, T.; Schramm, R. W.; Pientka, H. Separation and identification by thin layer chromatography of shikimic, quinic and cinnamic acids from legumes Acta Physiol. Plant 1981, 3, 69-75
28. Gaitonde, M. K.; Gordon, M. W. A microchemical method for the detection and determination of shikimic acid J. Biol. Chem. 1958, 230, 1043-1050
29. Mousdale, D. M.; Coggins, J. R. High-performance liquid chromatography of shikimate pathway intemediates J. Chromatogr. 1985, 329, 268-272 (Pubitemid 15038051)
30. Nandula, V. K.; Reddy, K. N.; Rimando, A. M.; Duke, S. O.; Poston, D. H. Glyphosate-resistant and -susceptible soybean (Glycine max) and canola (Brassica napus) dose response and metabolism relationships with glyphosate J. Agric. Food Chem. 2007, 55, 3540-3545 (Pubitemid 46806573)
31. Petersen, I. L.; Andersen, K. E.; Sørensen, J. C.; Sørensen, H. Determination of shikimate in crude plant extracts by micellar electrokinetic capillary chromatography. J. Chromatogr., A 2006, 1130, 253 - 258. (Pubitemid 44441318)
32. Mardones, C.; Hitschfeld, A.; Contreras, A.; Lepe, K.; Gutiérrez, L.; von Baer, D. Comparison of shikimic acid determination by capillary zone electrophoresis with direct and indirect detection with liquid chromatography for varietal differentiation of red wines J. Chromatogr., A 2005, 1085, 285-292 (Pubitemid 40994933)
33. Palmer, J. K.; List, D. M. Determination of organic acids in foods by liquid chromatography J. Agric. Food Chem. 1973, 21, 903-906
34. Lydon, J.; Duke, S. O. Glyphosate induction of elevated levels of hydroxybenzoic acids in higher plants J. Agric. Food Chem. 1988, 36, 813-818
35. Fischer, H. O. L.; Dangschat, G. Abbau der shikimisäure zur aconitsäure: 6. mitteilung über und derivate Helv. Chim. Acta 1935, 18, 1204-1206
36. Pline, W. A.; Wilcut, J. W.; Duke, S. O.; Edmisten, K. L.; Wells, R. Tolerance and accumulation of shikimic acid in response to glyphosate applications in glyphosate-resistant and nonglyphosate-resistant cotton (Gossypium hirsutum L.) J. Agric. Food Chem. 2002, 50, 506-512 (Pubitemid 34106670)
37. Cromartie, T. H.; Polge, N. D. Method of detecting shikimic acid. U.S. Patent 6,482,654, 2002.
38. Anonymous. Crop Protection Reference; C & P Press: New York, 2004; pp 1836 - 1855.
39. SigmaPlot. SigmaPlot® 11.2 User's Guide; Systat Software: San Jose, CA, 2010; p 890.
40. SAS, SAS procedures guide, version 8 ed.; SAS Institute, Inc.: Cary, NC, 2000; p 3884.
41. Muñoz-Rueda, A.; Gonzalez-Murua, C.; Becerril, J. M.; Sánchez-Díaz, M. F. Effects of glyphosate [ N -(phosphonomethyl) glycine] on photosynthetic pigments, stomatal response and photosynthetic electron transport in Medicago sativa and Trifolium pratense Physiol. Plant. 1986, 66, 63-68
42. Geiger, D. R.; Kapitan, S. W.; Tucci, M. A. Glyphosate inhibits photosynthesis and allocation of carbon starch in sugar beet leaves Plant Physiol. 1986, 82, 468-472
43. 2 and ethylene production and cellulase activity by glyphosate in Phaseolus vulgaris Weed Sci. 1979, 27, 103-106
44. Lee, T. T.; Dumas, T. Effects of glyphosate on indole-3-acetic acid metabolism in tolerant and susceptible plants J. Plant Growth Regul. 1985, 4, 29-39
45. Hernandez, A.; Garcia-Plazaola, J. I.; Becerril, J. M. Glyphosate effects on phenolic metabolism of nodulated soybean (Glycine max L. Merr.) J. Agric. Food Chem. 1999, 47, 2920-2925 (Pubitemid 29396381)
46. Campbell, W. F.; Evans, J. O.; Reed, S. C. Effects of glyphosate on chloroplast ultrastructure of quackgrass mesophyll cells Weed Sci. 1976, 24, 22-25
47. Uotila, M.; Evjen, K.; Iversen, T. H. The effects of glyphosate on the development and cell ultrastructure of white mustard (Sinapis alba L.) seedlings Weed Res. 1980, 20, 153-158
48. Mollenhauer, C.; Smart, C. C.; Amrhein, N. Glyphosate toxicity in the shoot apical region of the tomato plant. I. Plastid swelling is the initial ultrastructural feature following in vivo inhibition of 5-enolpyruvylshikimic acid 3-phosphate synthase Pestic. Biochem. Physiol. 1987, 29, 55-65 (Pubitemid 17148982)
49. Vaughn, K. C.; Duke, S. O. Ultrastructural effects of glyphosate on Glycine max seedlings Pestic. Biochem. Physiol. 1986, 26, 56-65 (Pubitemid 16056356)
50. Fuchs, M. A.; Geiger, D. R.; Reynolds, T. L.; Bourque, J. E. Mechanisms of glyphosate toxicity in velvetleaf (Abutilon theophrasti medikus) Pestic. Biochem. Physiol. 2002, 74, 27-39 (Pubitemid 36035031)
51. 4 dicot Amaranthus viridis Phytochemistry 1998, 48, 55-59 (Pubitemid 28242379)
52. de María, N.; Becerril, J. M.; García-Plazaola, J. I.; Hernandez, A.; De Felipe, M. R.; Fernandez-Pascual, M. New insights on glyphosate mode of action in nodular metabolism: role of shikimate accumulation J. Agric. Food Chem. 2006, 54, 2621-2628
53. Neera, G.; Garg, O. P. Effect of exogenous treatment with some phenolic compounds on nitrogen fixation, growth, and yield in Cicer arietinum L. (chickpea) Curr. Sci. 1989, 58, 31-32
54. Reddy, K. N.; Bellaloui, N.; Zablotowicz, R. M. Glyphosate effect on shikimate, nitrate reductase activity, yield, and seed composition in corn J. Agric. Food Chem. 2010, 58, 3646-3650
55. Anderson, K. A.; Cobb, W. T.; Loper, B. R. Analytical method for determination of shikimic acid: shikimic acid proportional to glyphosate application rates Commun. Soil Sci. Plant Anal. 2001, 32, 2831-2840 (Pubitemid 33091644)
56. Racchi, M. L.; Rebecchi, M.; Todesco, G.; Nielsen, E.; Forlani, G. Glyphosate tolerance in maize (Zea mays L.). 2. Selection and characterization of a tolerant somaclone Euphytica 1995, 82, 165-173
57. Wells, B. H.; Appleby, A. P. Lactofen increases glyphosate-stimulated shikimate production in little mallow (Malva parviflora) Weed Sci. 1992, 40, 171-173
58. Shaner, D. L.; Nadler-Hassar, T.; Henry, W. B.; Koger, C. H. A rapid in vivo shikimate accumulation assay with excised leaf discs Weed Sci. 2005, 53, 769-774 (Pubitemid 44298084)
59. Price, C. C.; Kroll, H. The kinetics of the periodate oxidation of 1,2-glycols J. Am. Chem. Soc. 1938, 60, 2726-2729
60. Price, C. C.; Knell, M. The kinetics of the periodate oxidation of 1,2-glycols. II. Ethylene glycol, pinacol and cis-and trans -cyclohexene glycols J. Am. Chem. Soc. 1942, 64, 552-554
61. Mossor, T.; Schramm, R. W. Colorimetric assay of shikimic acid against quinic acid Anal. Biochem. 1972, 47, 39-45
62. Yoshida, S.; Hasegawa, M. A microcolorimetric method for the determination of shikimic acid Arch. Biochem. Biophys. 1957, 70, 377-381
63. Saslaw, L. D.; Waravdekar, V. S. A colorimetric method of estimation of shikimic acid Biochim. Biophys. Acta 1960, 37, 367-368
64. Mullican, R. C. A thiobarbituric assay for shikimic acid Anal. Biochem. 1963, 6, 181-192
65. Cromartie, T. H.; Polge, N. D. An improved assay for shikimic acid and its use as a monitor for the activity of sulfosate Proc. Weed Sci. Soc. Am. 2000, 40, 291
66. Bonner, C. A.; Jensen, R. A. Cloning of cDNA encoding the bifunctional dehydroquinase. Shikimate dehydrogenase of aromatic-amino-acid biosynthesis in Nicotiana tabacum Biochem. J. 1994, 302, 11-14 (Pubitemid 24256329)
67. Leuschner, C.; Herrmann, K. M.; Schultz, G. The metabolism of quinate in pea roots. Purification and partial characterization of a quinate hydrolyase Plant Physiol. 1995, 108, 319-325
68. Bouchez-Mahiout, I.; Doyen, C.; Lauriere, M. Accurate detection of both glycoproteins and total proteins on blots: control of side reactions occurring after periodate oxidation of proteins Electrophoresis 1999, 20, 1412-1417 (Pubitemid 29299988)
69. Kim, U. J.; Kuga, S.; Wada, M.; Okano, T.; Kondo, T. Periodate oxidation of crystalline cellulose Biomacromolecules 2000, 1, 488-492
70. Kawakami, T.; Akaji, K.; Aimoto, S. Peptide bond formation mediated by 4,5-dimethoxy-2-mercaptobenzylamine after periodate oxidation of the N-terminal serine residue Org. Lett. 2001, 3, 1403-1405 (Pubitemid 33629476)
71. Hage, D. S.; Wolfe, C. A.; Oates, M. R. Development of a kinetic model to describe the effective rate of antibody oxidation by periodate Bioconjugate Chem. 1997, 8, 914-920 (Pubitemid 27526421)
72. De Bank, P. A.; Kellam, B.; Kendall, D. A.; Shakesheff, K. M. Surface engineering of living myoblasts via selective periodate oxidation Biotechnol. Bioeng. 2003, 81, 800-808 (Pubitemid 36313718)
73. Brooks, B. R.; Brooks, C. L. R.; Mackerell, A. D. J.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-1614
74. Aalmo, K. M.; Painter, T. J. Periodate oxidation of methyl glycopyranosides: rate coefficients and relative stabilities of intermediate hemiacetals Carbohydr. Res. 1981, 89, 73-82
75. Reddy, K. N.; Rimando, A. M.; Duke, S. O.; Nandula, V. K. Aminomethylphosphonic acid accumulation in plant species treated with glyphosate J. Agric. Food Chem. 2008, 56, 2125-2130 (Pubitemid 351497876)