Plants as biofactories: Glyphosate-induced production of shikimic acid and phenolic antioxidants in wounded carrot tissue

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 45, 2012, Pages 11378-11386

  Becerra Moreno, Alejandro ^a   Benavides, Jorge ^a   Cisneros Zevallos, Luis ^b   Jacobo Velázquez, Daniel A ^a  

^a SCHOOL OF ENGINEERING AND SCIENCES   (Mexico)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

carrot; glyphosate; phenolic compounds; postharvest abiotic stresses; shikimic acid; wounding

Indexed keywords

BIOHAZARDS; CARBOXYLIC ACIDS; CHEMICAL COMPOUNDS; GENETIC ENGINEERING; HERBICIDES; METABOLITES; PHENOLS; TISSUE;

ABIOTIC STRESS; CARROT; GLYPHOSATES; PHENOLIC COMPOUNDS; SHIKIMIC ACIDS; WOUNDING;

GENETICALLY MODIFIED PLANTS;

EID: 84869192335     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf303252v     Document Type: Article

References (49)

1. Ye, X.; Al-Babili, S.; Klöti, A.; Zhang, J.; Lucca, P.; Beyer, P.; Potrykus, I. Engineering the provitamin A (β-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm Science 2000, 287, 303-305
2. Niggeweg, R.; Michael, A. J.; Martin, C. Engineering plants with increased levels of the antioxidant chlorogenic acid Nat. Biotechnol. 2004, 22, 746-754
3. Johansson, L.; Lindskog, A.; Silfversparre, G.; Cimander, C.; Nielsen, K. F.; Lidén, G. Shikimic acid production by a modified strain of E. coli (W3110.shik1) under phosphate-limited and carbon-limited conditions Biotechnol. Bioeng. 2005, 92, 541-552
4. Diretto, G.; Al-Babili, S.; Tavazza, R.; Papacchioli, V.; Beyer, P.; Giuliano, G. Metabolic engineering of potato carotenoid content through tuber-specific over expression of a bacterial mini-pathway PLoS ONE 2007, 2, e350
5. Colwell, R. K.; Norse, E. A.; Pimentel, D.; Sharples, F. E.; Simberloff, D. Genetic engineering in agriculture Science 1985, 229, 111-112
6. Cisneros-Zevallos, L. The use of controlled postharvest abiotic stresses as a tool for enhancing the nutraceutical content and adding-value of fresh fruits and vegetables J. Food Sci. 2003, 68, 1560-1565
7. Surjadinata, B. B. Wounding and Ultraviolet Radiation Stresses Affect the Phenolic Profile and Antioxidant Capacity of Carrot Tissue. Ph.D. dissertation, Texas A&M University, College Station, TX, 2006.
8. Heredia, J. B.; Cisneros-Zevallos, L. The effect of exogenous ethylene and methyl jasmonate on pal activity, phenolic profiles and antioxidant capacity of carrots (Daucus carota) under different wounding intensities Postharvest Biol. Technol. 2009, 51, 242-249
9. Heredia, J. B.; Cisneros-Zevallos, L. The effect of exogenous ethylene and methyl jasmonate on the accumulation of phenolic antioxidants in selected whole and wounded fresh produce Food Chem. 2009, 115, 1500-1508
10. Jacobo-Velázquez, D. A.; Cisneros-Zevallos, L. Correlations of antioxidant activity against phenolic content revisited: A new approach in data analysis for food and medicinal plants J. Food Sci. 2009, 74, R107-R113
11. Jacobo-Velázquez, D. A.; Martínez-Hernández, G. B.; Rodríguez, S.; Cao, C.-M.; Cisneros-Zevallos, L. Plants as biofactories: Physiological role of reactive oxygen species on the accumulation of phenolic antioxidants in carrot tissue under wounding and hyperoxia stress J. Agric. Food Chem. 2011, 59, 6583-6593
12. Surjadinata, B. B.; Cisneros-Zevallos, L. Biosynthesis of phenolic antioxidants in carrot tissue increases with wounding intensity Food Chem. 2012, 134, 615-624
13. Robinson, W. E., Jr.; Cordeiro, M.; Abdel-Malek, S.; Jia, Q.; Chow, S. A.; Reinecke, M. G.; Mitchell, W. M. Dicaffeoylquinic acid inhibitors of human immunodeficiency virus integrase: inhibition of the core catalytic domain of human immunodeficiency virus integrase Mol. Pharmacol. 1996, 50, 845-855
14. Zhu, K.; Cordeiro, M. L.; Atienza, J.; Robinson, W. E., Jr.; Chow, S. A. Irreversible inhibition of human immunodeficiency virus type 1 integrase by dicaffeoylquinic acids J. Virol. 1999, 73, 3309-3316
15. Kim, S.-S.; Park, R.-Y.; Jeon, H.-J.; Kwon, Y.-S.; Chun, W. Neuroprotective effect of 3,5-dicaffeoylquinic acid on hydrogen peroxide-induced cell death in SH-SY5Y cells Phytother. Res. 2005, 19, 243-245
16. Thom, E. The effect of chlorogenic acid enriched coffee on glucose absorption in healthy volunteers and its effect on body mass when used long-term in overweight and obese people J. Int. Med Res. 2007, 35, 900-908
17. Wang, G.-F.; Shi, L.-P.; Ren, Y.-D.; Liu, Q.-F.; Liu, H.-.F.; Zhang, R.-J.; Li, Z.; Zhu, F.-H.; He, P.-L.; Tang, W.; Tao, P.-Z.; Li, C.; Zhao, W.-M.; Zuo, J.-P. Anti-hepatitis B virus activity of chlorogenic acid, quinic acid and caffeic acid in vitro and in vivo Antivir. Res. 2009, 83, 186-190
18. Dyer, W. E.; Henstrand, J. M.; Handa, A. K.; Herrmann, K. M. Wounding induces the first enzyme of the shikimate pathway in Solanaceae Proc. Natl. Acad. Sci. U.S.A. 1989, 86, 7370-7373
19. Sharma, R.; Jain, M.; Bhatnagar, R. K.; Bhalla-Sarin, N. Differential expression of DAHP synthase and chorismate mutase in various organs of Brassica juncea and the effect of external factors on enzyme activity Physiol. Plant. 1999, 105, 739-745
20. Jacobo-Velázquez, D. A.; Cisneros-Zevallos, L. An alternative use of horticultural crops: stressed plants as biofactories of bioactive phenolic compounds Agriculture 2012, 2, 259-271
21. Farina, V.; Brown, J. D. Tamiflu: the supply problem Angew. Chem., Int. Ed. 2006, 45, 7330-7334
22. Martin, E.; Duke, J.; Pelkki, M.; Clausen, E. C.; Carrier, D. J. Sweetgum (Liquidambar styraciflua L.): extraction of shikimic acid coupled to dilute acid pretreatment Appl. Biochem. Biotechnol. 2010, 162, 1660-1668
23. Bochkov, D. V.; Sysolyatin, S. V.; Kalashnikov, A. I.; Surmacheva, I. A. Shikimic acid: review of its analytical, isolation, and purification techniques from plant and microbial sources J. Chem. Biol. 2012, 5, 5-17
24. Davis, B. D. Aromatic biosynthesis. I. The role of shikimic acid J. Biol. Chem. 1951, 191, 315-325
25. Amrhein, N.; Deus, B.; Gehrke, P.; Steinrücken, H. C. The site of the 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
26. 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
27. Lydon, J.; Duke, S. O. Glyphosate induction of elevated levels of hydroxybenzoic acids in higher plants J. Agric. Food Chem. 1988, 36, 813-818
28. Dewick, P. M. Medicinal natural products: A Biosynthetic Approach; Wiley: New York, 2009; pp 539.
29. Bradberry, S. M.; Proudfoot, A. T.; Vale, J. A. Glyphosate poisoning Toxicol. Rev. 2004, 23, 159-167
30. Zelaya, I. A.; Anderson, J. A.; Owen, M. D.; Landes, R. D. Evaluation of spectrophotometric and HPLC methods for shikimic acid determination in plants: models in glyphosate-resistant and susceptible crops J. Agric. Food Chem. 2011, 59, 2202-2212
31. Tumbas, V. T.; Mandić, A. I.; Ćetković, G. S.; Ailas, S. M.; Čanadanović-Brunet, J. M. HPLC analysis of phenolic acids in mountain germander (Teucrium montanum L.) extracts Acta Periodica Technol. 2004, 35, 265-273
32. Yao, L. H.; Jiang, Y. M.; Datta, N.; Singanusong, R.; Liu, X.; Duan, J.; Raymont, K.; Lisle, A.; Xu, Y. HPLC analyses of flavanols and phenolic acids in the fresh young shoots of tea (Camellia sinensis) grown in Australia Food Chem. 2004, 84, 253-263
33. Dobberstein, D.; Bunzel, M. Separation and detection of cell wall-bound ferulic acid dehydrodimers and dehydrotrimers in cereals and other plant materials by reversed phase high-performance liquid chromatography with ultraviolet detection J. Agric. Food Chem. 2010, 58, 8927-8935
34. Laghari, A. H.; Memon, S.; Nelofar, A.; Khan, K. M.; Yasmin, A. Determination of free phenolic acids and antioxidant activity of methanol extracts obtained from fruits and leaves of Chenopodium album Food Chem. 2011, 126, 1850-1855
35. Zhang, D.; Hamauzu, Y. Phenolic compounds and their antioxidant properties in different tissues of carrots (Daucus carota L.) J. Food Agric. Environ. 2004, 2, 95-100
36. Weaver, L. M.; Herrmann, K. M. Dynamics of the shikimate pathway in plants Trends Plant Sci. 1997, 2, 346-351
37. Herrmann, K. M.; Weaver, L. M. The shikimate pathway Annu. Rev. Plant Physiol. 1999, 50, 473-503
38. Holländer-Czytko, H.; Amrhein, N. Subcellular compartment 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
39. Orozco-Cárdenas, M. L.; Narváez-Vásquez, J.; Ryan, C. A. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate Plant Cell 2001, 13, 179-191
40. Song, C. J.; Steinebrunner, I.; Wang, X.; Stout, S. C.; Roux, S. J. Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis Plant Physiol. 2006, 140, 1222-1232
41. 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
42. Marchiosi, R.; Ferrarese, M. L. L.; Bonini, E. A.; Fernandes, N. G.; Ferro, A. P.; Ferrarese-Filho, O. Glyphosate-induced metabolic changes in susceptible and glyphosate-resistant soybean (Glycine max L.) roots Pestic. Biochem. Phys. 2009, 93, 38-33
43. Holländer, H.; Amrhein, N. The site of the inhibition of the shikimate pathway by glyphosate. I. Inhibition by glyphosate of phenylpropanoid synthesis in buckwheat (Fagopyrum esculentum moench) Plant Physiol. 1980, 66, 823-829
44. Rittinger, P. A.; Biggs, A. R.; Peirson, D. R. Histochemistry of lignin and suberin deposition in boundary layers formed after wounding in various plant species and organs Can. J. Bot. 1987, 65, 1886-1892
45. Menin, B.; Comino, C.; Moglia, A.; Dolzhenko, Y.; Portis, E.; Lanteri, S. Identification and mapping of genes related to caffeoylquinic acid synthesis in Cynara cardunculus L Plant Sci. 2010, 179, 338-347
46. Hanson, K. R.; Zucker, M. The biosynthesis of chlorogenic acids and related conjugates of the hydroxycinnamic acids J. Biol. Chem. 1963, 238, 1105-1115
47. Duke, S. O.; Hoagland, R. E.; Elmore, C. D. Effects of glyphosate on metabolism of phenolic compounds. V. l-α-Aminooxy-β-phenylpropionic acid and glyphosate effects on phenylalanine ammonia-lyase in soybean seedlings Plant Physiol. 1980, 65, 17-21
48. Mattila, P.; Kumpulainen, J. Determination of free and total phenolic acids in plant-derived foods by HPLC with diode-array detection J. Agric. Food Chem. 2002, 50, 3660-3667
49. Jacobo-Velázquez, D. A. Physiological and Molecular Mechanisms Governing the Postharvest Stress-Induced Accumulation of Antioxidant Phenolic Compounds in Carrots. Ph.D. dissertation, Texas A&M University, College Station, TX, 2010.