Rapid Phytotransformation of Benzotriazole Generates Synthetic Tryptophan and Auxin Analogs in Arabidopsis

Environmental Science and Technology

Volumn 49, Issue 18, 2015, Pages 10959-10968

  LeFevre, Gregory H ^a,b   Müller, Claudia E ^a,b   Li, Russell Jingxian ^a   Luthy, Richard G ^a,b   Sattely, Elizabeth S ^a,b  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; BIOSYNTHESIS; ENDOCRINOLOGY; HORMONES; METABOLITES; WASTEWATER RECLAMATION;

AQUATIC ENVIRONMENTS; BIOLOGICAL EFFECTS; BIOSYNTHETIC ENZYMES; BIOSYNTHETIC PATHWAY; HYDROPONIC SYSTEMS; PHYTOTRANSFORMATION; PRODUCT VERIFICATION; TRANSFORMATION PRODUCTS;

AMINO ACIDS;

AMINO ACID; AUXIN; BENZOTRIAZOLE DERIVATIVE; PHYTOHORMONE; TRYPTOPHAN; BENZOTRIAZOLE; INDOLEACETIC ACID DERIVATIVE; TRIAZOLE DERIVATIVE;

AMINO ACID; AQUATIC ENVIRONMENT; BIOTRANSFORMATION; CHEMICAL COMPOUND; ENVIRONMENTAL EFFECT; HERB; HORMONE; METABOLITE; STORMWATER; XENOBIOTICS;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; GLYCOSYLATION; HYDROPONICS; METABOLOMICS; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; QUADRUPOLE MASS SPECTROMETRY; TIME OF FLIGHT MASS SPECTROMETRY; BIOREMEDIATION; CHEMISTRY; METABOLISM; METABOLOME; TIME FACTOR;

ARABIDOPSIS;

ARABIDOPSIS; BIODEGRADATION, ENVIRONMENTAL; GLYCOSYLATION; HYDROPONICS; INDOLEACETIC ACIDS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; TIME FACTORS; TRIAZOLES; TRYPTOPHAN;

EID: 84941695604     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b02749     Document Type: Article

References (83)

1. Matthews, J. H.; Wickel, B. A. J.; Freeman, S. Converging Currents in Climate-Relevant Conservation: Water, Infrastructure, and Institutions PLoS Biol. 2011, 9, e1001159 10.1371/journal.pbio.1001159
2. Bischel, H. N.; Simon, G. L.; Frisby, T. M.; Luthy, R. G. Management Experiences and Trends for Water Reuse Implementation in Northern California Environ. Sci. Technol. 2012, 46, 180-188 10.1021/es202725e
3. Eggen, R. I. L.; Hollender, J.; Joss, A.; Schärer, M.; Stamm, C. Reducing the discharge of micropollutants in the aquatic environment: the benefits of upgrading wastewater treatment plants Environ. Sci. Technol. 2014, 48, 7683-7689 10.1021/es500907n
4. Loos, R.; Carvalho, R.; António, D. C.; Comero, S.; Locoro, G.; Tavazzi, S.; Paracchini, B.; Ghiani, M.; Lettieri, T.; Blaha, L.; Jarosova, B.; Voorspoels, S.; Servaes, K.; Haglund, P.; Fick, J.; Lindberg, R. H.; Schwesig, D.; Gawlik, B. M. EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents Water Res. 2013, 47, 6475-6487 10.1016/j.watres.2013.08.024
5. Musolff, A.; Leschik, S.; Reinstorf, F.; Strauch, G.; Schirmer, M. Micropollutant Loads in the Urban Water Cycle Environ. Sci. Technol. 2010, 44, 4877-4883 10.1021/es903823a
6. Goldstein, M.; Shenker, M.; Chefetz, B. Insights into the Uptake Processes of Wastewater-Borne Pharmaceuticals by Vegetables Environ. Sci. Technol. 2014, 48, 5593-5600 10.1021/es5008615
7. Malchi, T.; Maor, Y.; Tadmor, G.; Shenker, M.; Chefetz, B. Irrigation of Root Vegetables with Treated Wastewater: Evaluating Uptake of Pharmaceuticals and the Associated Human Health Risks Environ. Sci. Technol. 2014, 48, 9325-9333 10.1021/es5017894
8. Wu, X.; Conkle, J. L.; Ernst, F.; Gan, J. Treated Wastewater Irrigation: Uptake of Pharmaceutical and Personal Care Products by Common Vegetables under Field Conditions Environ. Sci. Technol. 2014, 48, 11286-11293 10.1021/es502868k
9. Macherius, A.; Eggen, T.; Lorenz, W.; Moeder, M.; Ondruschka, J.; Reemtsma, T. Metabolization of the Bacteriostatic Agent Triclosan in Edible Plants and its Consequences for Plant Uptake Assessment Environ. Sci. Technol. 2012, 46, 10797-10804 10.1021/es3028378
10. Qu, S.; Kolodziej, E. P.; Long, S. A.; Gloer, J. B.; Patterson, E. V.; Baltrusaitis, J.; Jones, G. D.; Benchetler, P. V.; Cole, E. A.; Kimbrough, K. C.; Tarnoff, M. D.; Cwiertny, D. M. Product-to-Parent Reversion of Trenbolone: Unrecognized Risks for Endocrine Disruption Science 2013, 342, 347-351 10.1126/science.1243192
11. Janna, H.; Scrimshaw, M. D.; Williams, R. J.; Churchley, J.; Sumpter, J. P. From Dishwasher to Tap? Xenobiotic Substances Benzotriazole and Tolyltriazole in the Environment Environ. Sci. Technol. 2011, 45, 3858-3864 10.1021/es103267g
12. Dummer, N. 4(5)-Methylbenzotriazole: a review of the life-cycle of an emerging contaminant Rev. Environ. Sci. Bio/Technol. 2014, 13, 53-61 10.1007/s11157-013-9318-y
13. Kiss, A.; Fries, E. Seasonal source influence on river mass flows of benzotriazoles J. Environ. Monit. 2012, 14 (2) 697-703 10.1039/c2em10826g
14. Corsi, S. R.; Zitomer, D. H.; Field, J. A.; Cancilla, D. A. Nonylphenol Ethoxylates and Other Additives in Aircraft Deicers, Antiicers, and Waters Receiving Airport Runoff Environ. Sci. Technol. 2003, 37, 4031-4037 10.1021/es034005i
15. Busetti, F.; Ruff, M.; Linge, K. L. Target screening of chemicals of concern in recycled water Environ. Sci.: Water Res. Technol. 2015, 10.1039/C4EW00104D
16. Loi, C. H.; Busetti, F.; Linge, K. L.; Joll, C. A. Development of a solid-phase extraction liquid chromatography tandem mass spectrometry method for benzotriazoles and benzothiazoles in wastewater and recycled water Journal of Chromatography A 2013, 1299, 48-57 10.1016/j.chroma.2013.04.073
17. Reemtsma, T.; Miehe, U.; Duennbier, U.; Jekel, M. Polar pollutants in municipal wastewater and the water cycle: Occurrence and removal of benzotriazoles Water Res. 2010, 44, 596-604 10.1016/j.watres.2009.07.016
18. Liu, Y.; Ying, G.; Shareef, A.; Kookana, R. S. Biodegradation of three selected benzotriazoles under aerobic and anaerobic conditions Water Res. 2011, 45, 5005-5014 10.1016/j.watres.2011.07.001
19. Herzog, B.; Lemmer, H.; Huber, B.; Horn, H.; Müller, E. Xenobiotic benzotriazoles-Biodegradation under meso- and oligotrophic conditions as well as denitrifying, sulfate-reducing, and anaerobic conditions Environ. Sci. Pollut. Res. 2014, 21, 2795-2804 10.1007/s11356-013-2199-3
20. Huntscha, S.; Hofstetter, T. B.; Schymanski, E. L.; Spahr, S.; Hollender, J. Biotransformation of Benzotriazoles: Insights from Transformation Product Identification and Compound-Specific Isotope Analysis Environ. Sci. Technol. 2014, 48, 4435-4443 10.1021/es405694z
21. Liu, Y.; Ying, G.; Shareef, A.; Kookana, R. S. Biodegradation of three selected benzotriazoles in aquifer materials under aerobic and anaerobic conditions J. Contam. Hydrol. 2013, 151, 131-139 10.1016/j.jconhyd.2013.05.006
22. Janssen, E. M. L.; Marron, E.; McNeill, K. Aquatic photochemical kinetics of benzotriazole and structurally related compounds Environ. Sci.: Processes Impacts 2015, 17, 939-946 10.1039/C5EM00045A
23. Bahnmüller, S.; Loi, C. H.; Linge, K. L.; Gunten, U. v.; Canonica, S. Degradation rates of benzotriazoles and benzothiazoles under UV-C irradiation and the advanced oxidation process UV/H2O2 Water Res. 2015, 74, 143-154 10.1016/j.watres.2014.12.039
24. Mawhinney, D. B.; Vanderford, B. J.; Snyder, S. A. Transformation of 1H-Benzotriazole by Ozone in Aqueous Solution Environ. Sci. Technol. 2012, 46, 7102-7111 10.1021/es300338e
25. Heeb, F.; Singer, H.; Pernet-Coudrier, B.; Qi, W.; Liu, H.; Longrée, P.; Müller, B.; Berg, M. Organic micropollutants in rivers downstream of the megacity Beijing: Sources and mass fluxes in a large-scale wastewater irrigation system Environ. Sci. Technol. 2012, 46, 8680-8688 10.1021/es301912q
26. Giger, W.; Schaffner, C.; Kohler, H. E. Benzotriazole and Tolyltriazole as Aquatic Contaminants. 1. Input and Occurrence in Rivers and Lakes Environ. Sci. Technol. 2006, 40, 7186-7192 10.1021/es061565j
27. Kolpin, D. W.; Furlong, E. T.; Meyer, M. T.; Thurman, E. M.; Zaugg, S. D.; Barber, L. B.; Buxton, H. T. Pharmaceuticals, Hormones, and Other Organic Wastewater Contaminants in U.S. Streams, 1999-2000: A National Reconnaissance Environ. Sci. Technol. 2002, 36, 1202-1211 10.1021/es011055j
28. Lai, H.; Ying, G.; Ma, Y.; Chen, Z.; Chen, F.; Liu, Y. Occurrence and dissipation of benzotriazoles and benzotriazole ultraviolet stabilizers in biosolid-amended soils Environ. Toxicol. Chem. 2014, 33, 761-767 10.1002/etc.2498
29. Asimakopoulos, A. G.; Bletsou, A. A.; Wu, Q.; Thomaidis, N. S.; Kannan, K. Determination of Benzotriazoles and Benzothiazoles in Human Urine by Liquid Chromatography-Tandem Mass Spectrometry Anal. Chem. 2013, 85, 441-448 10.1021/ac303266m
30. Wang, L.; Asimakopoulos, A. G.; Moon, H.; Nakata, H.; Kannan, K. Benzotriazole, Benzothiazole, and Benzophenone Compounds in Indoor Dust from the United States and East Asian Countries Environ. Sci. Technol. 2013, 47, 4752-4759 10.1021/es305000d
31. Seeland, A.; Oetken, M.; Kiss, A.; Fries, E.; Oehlmann, J. Acute and chronic toxicity of benzotriazoles to aquatic organisms Environ. Sci. Pollut. Res. 2012, 19, 1781-1790 10.1007/s11356-011-0705-z
32. Corsi, S. R.; Geis, S. W.; Loyo-Rosales, J.; Rice, C. P. Aquatic Toxicity of Nine Aircraft Deicer and Anti-Icer Formulations and Relative Toxicity of Additive Package Ingredients Alkylphenol Ethoxylates and 4,5-Methyl-1H-benzotriazoles Environ. Sci. Technol. 2006, 40, 7409-7415 10.1021/es0603608
33. Harris, C. A.; Routledge, E. J.; Schaffner, C.; Brian, J. V.; Giger, W.; Sumpter, J. P. Benzotriazole is antiestrogenic in vitro but not in vivo Environ. Toxicol. Chem. 2007, 26, 2367-2372 10.1897/06-587R.1
34. Tangtian, H.; Bo, L.; Wenhua, L.; Shin, P. K. S.; Wu, R. S. S. Estrogenic potential of benzotriazole on marine medaka (Oryzias melastigma) Ecotoxicol. Environ. Saf. 2012, 80, 327-332 10.1016/j.ecoenv.2012.03.020
35. Cancilla, D. A.; Holtkamp, A.; Matassa, L.; Fang, X. Isolation and characterization of Microtox®-active components from aircraft de-icing/anti-icing fluids Environ. Toxicol. Chem. 1997, 16, 430-434 10.1002/etc.5620160306
36. Nagayoshi, H.; Kakimoto, K.; Takagi, S.; Konishi, Y.; Kajimura, K.; Matsuda, T. Benzotriazole Ultraviolet Stabilizers Show Potent Activities as Human Aryl Hydrocarbon Receptor Ligands Environ. Sci. Technol. 2015, 49, 578-587 10.1021/es503926w
37. U.S. EPA Drinking Water Contaminants: National Primary Drinking Water Regulations. U.S. EPA website, http://water.epa.gov/drink/contaminants/index.cfm. Accessed 2015.
38. McCutcheon, S. C.; Schnoor, J. L., Eds.; In Phytoremediation: Transformation and Control of Contaminants; John Wiley and Sons: Hoboken, NJ, 2003; pp 987.
39. Castro, S.; Davis, L. C.; Erickson, L. E. Temperature and pH Effects on Plant Uptake of Benzotriazoles by Sunflowers in Hydroponic Culture Int. J. Phytorem. 2004, 6, 209-225 10.1080/16226510490496384
40. Chen, Y.; Xu, W.; Shen, H.; Yan, H.; Xu, W.; He, Z.; Ma, M. Engineering Arsenic Tolerance and Hyperaccumulation in Plants for Phytoremediation by a PvACR3 Transgenic Approach Environ. Sci. Technol. 2013, 47, 9355-9362 10.1021/es4012096
41. Mashiguchi, K.; Tanaka, K.; Sakai, T.; Sugawara, S.; Kawaide, H.; Natsume, M.; Hanada, A.; Yaeno, T.; Shirasu, K.; Yao, H.; McSteen, P.; Zhao, Y.; Hayashi, K.; Kamiya, Y.; Kasahara, H. The main auxin biosynthesis pathway in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 18512-18517 10.1073/pnas.1108434108
42. Su, Z.; Xu, Z.; Peng, R.; Tian, Y.; Zhao, W.; Han, H.; Yao, Q.; Wu, A. Phytoremediation of Trichlorophenol by Phase II Metabolism in Transgenic Arabidopsis Overexpressing a Populus Glucosyltransferase Environ. Sci. Technol. 2012, 46, 4016-4024 10.1021/es203753b
43. + at Sublethal Concentrations Environ. Sci. Technol. 2013, 47, 5442-5449 10.1021/es4004334
44. LeFevre, G. H.; Hozalski, R. M.; Novak, P. J. Root Exudate Enhanced Contaminant Desorption: An Abiotic Contribution to the Rhizosphere Effect Environ. Sci. Technol. 2013, 47, 11545-11553 10.1021/es402446v
45. Eaton, A. D.; Clesceri, L. S.; Grennber, A. E. Standard Methods for the Examination of Water and Wastewater. APHA, AWWA, WEF: Washington, D.C., 1995; pp 1082.
46. Smith, C. A.; Want, E. J.; OMaille, G.; Abagyan, R.; Siuzdak, G. XCMS: Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification Anal. Chem. 2006, 78, 779-787 10.1021/ac051437y
47. De Vos, R.C.H.; Moco, S.; Lommen, A.; Keurentjes, J. J. B.; Bino, R. J.; Hall, R. D. Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry Nat. Protoc. 2007, 2, 778-791 10.1038/nprot.2007.95
48. Schymanski, E. L.; Jeon, J.; Gulde, R.; Fenner, K.; Ruff, M.; Singer, H. P.; Hollender, J. Identifying Small Molecules via High Resolution Mass Spectrometry: Communicating Confidence Environ. Sci. Technol. 2014, 48, 2097-2098 10.1021/es5002105
49. Gerhardt, K. E.; Huang, X.; Glick, B. R.; Greenberg, B. M. Phytoremediation and rhizoremediation of organic soil contaminants: Potential and challenges Plant Sci. 2009, 176, 20-30 10.1016/j.plantsci.2008.09.014
50. Jacobson, M. E.; Chiang, S. Y.; Gueriguian, L.; Westholm, L. R.; Pierson, J.; Zhu, G.; Saunders, F. M. Transformation Kinetics of Trinitrotoluene Conversion in Aquatic Plants. In Phytoremediation; John Wiley & Sons, Inc.: 2003; pp 409-427.
51. Badalucco, L.; Nannipieri, P. Nutrient Transformations in the Rhizosphere. In The Rhizosphere; CRC Press: Boca Raton, FL, 2007; pp 111-133.
52. Jones, D. L.; Darrah, P. R. Influx and efflux of amino acids from Zea mays L. roots and their implications for N nutrition and the rhizosphere Plant Soil 1993, 155-156, 87-90 10.1007/BF00024990
53. Jones, D. L.; Darrah, P. R. Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere Plant Soil 1994, 163, 1-12
54. Dettenmaier, E. M.; Doucette, W. J.; Bugbee, B. Chemical Hydrophobicity and Uptake by Plant Roots Environ. Sci. Technol. 2009, 43, 324-329 10.1021/es801751x
55. Briggs, G. G.; Rigitano, R. L.; Bromilow, R. H. Physico-chemical factors affecting uptake by roots and translocation to shoots of weak acids in barley Pestic. Sci. 1987, 19, 101-112 10.1002/ps.2780190203
56. Wang, H.; Burda, C.; Persy, G.; Wirz, J. Photochemistry of 1H-Benzotriazole in Aqueous Solution: A Photolatent Base J. Am. Chem. Soc. 2000, 122, 5849-5855 10.1021/ja994464c
57. Schwitzguébel, J.; Vanek, T. Some Fundamental Advances for Xenobiotic Chemicals. In Phytoremediation; John Wiley & Sons, Inc.: Hoboken, NJ, 2003; pp 121-157.
58. Burken, J. G. Uptake and Metabolism of Organic Compounds: Green-Liver Model. In Phytoremediation; John Wiley & Sons, Inc.: Hoboken, NJ, 2003; pp 59-84.
59. Coleman, J.; Blake-Kalff, M.; Davies, E. Detoxification of xenobiotics by plants: chemical modification and vacuolar compartmentation Trends Plant Sci. 1997, 2, 144-151 10.1016/S1360-1385(97)01019-4
60. Sandermann, H., Jr Plant metabolism of xenobiotics Trends Biochem. Sci. 1992, 17, 82-84 10.1016/0968-0004(92)90507-6
61. Riechers, D. E.; Kreuz, K.; Zhang, Q. Detoxification without Intoxication: Herbicide Safeners Activate Plant Defense Gene Expression Plant Physiol. 2010, 153, 3-13 10.1104/pp.110.153601
62. Zhai, G.; Gutowski, S. M.; Lehmler, H.; Schnoor, J. L. Enantioselective Transport and Biotransformation of Chiral OH-PCBs in Whole Poplar Plants Environ. Sci. Technol. 2014, 48, 12213-12220 10.1021/es503443e
63. Colby, S. R. Herbicide Metabolism: N-Glycoside of Amiben Isolated from Soybean Plants Science 1965, 150, 619-620 10.1126/science.150.3696.619
64. Winkler, R.; Sandermann, H. N-Glucosyl conjugates of chlorinated anilines: spontaneous formation and cleavage J. Agric. Food Chem. 1992, 40, 2008-2012 10.1021/jf00022a054
65. Zhai, G.; Lehmler, H.; Schnoor, J. L. Inhibition of Cytochromes P450 and the Hydroxylation of 4-Monochlorobiphenyl in Whole Poplar Environ. Sci. Technol. 2013, 47, 6829-6835 10.1021/es304298m
66. Zhai, G.; Lehmler, F.; Schnoor, J. L. Identification of hydroxylated metabolites of 3,3 ′,4,4 ′-tetrachlorobiphenyl and metabolic pathway in whole poplar plants Chemosphere 2010, 81, 523-528 10.1016/j.chemosphere.2010.07.036
67. Williamson, G. Common Features in the Pathways of Absorption and Metabolism of Flavonoids. In Phytochemicals; CRC Press: Boca Raton, FL, 2003, chapter 2.
68. Radwanski, E. R.; Last, R. L. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics Plant Cell 1995, 7, 921-934 10.2307/3870047
69. Korasick, D. A.; Enders, T. A.; Strader, L. C. Auxin biosynthesis and storage forms J. Exp. Bot. 2013, 64, 2541-2555 10.1093/jxb/ert080
70. Woodward, A. W.; Bartel, B. Auxin: regulation, action, and interaction Ann. Bot. 2005, 95, 707-735 10.1093/aob/mci083
71. Zhao, Y. Auxin Biosynthesis and Its Role in Plant Development Annu. Rev. Plant Biol. 2010, 61, 49-64 10.1146/annurev-arplant-042809-112308
72. Won, C.; Shen, X.; Mashiguchi, K.; Zheng, Z.; Dai, X.; Cheng, Y.; Kasahara, H.; Kamiya, Y.; Chory, J.; Zhao, Y. Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 18518-18523 10.1073/pnas.1108436108
73. Zhao, Y.; Christensen, S. K.; Fankhauser, C.; Cashman, J. R.; Cohen, J. D.; Weigel, D.; Chory, J. A Role for Flavin Monooxygenase-Like Enzymes in Auxin Biosynthesis Science 2001, 291, 306-309 10.1126/science.291.5502.306
74. Karp, P. D.; Ouzounis, C. A.; Moore-Kochlacs, C.; Goldovsky, L.; Kaipa, P.; Ahrén, D.; Tsoka, S.; Darzentas, N.; Kunin, V.; López-Bigas, N. Expansion of the BioCyc collection of pathway/genome databases to 160 genomes Nucleic Acids Res. 2005, 33, 6083-6089 10.1093/nar/gki892
75. Seidel, C.; Walz, A.; Park, S.; Cohen, J. D.; Ludwig-Muller, J. Indole-3-acetic acid protein conjugates: novel players in auxin homeostasis Plant Biol. (Berlin, Ger.) 2006, 8, 340-345 10.1055/s-2006-923802
76. Rentsch, D.; Schmidt, S.; Tegeder, M. Transporters for uptake and allocation of organic nitrogen compounds in plants FEBS Lett. 2007, 581, 2281-2289 10.1016/j.febslet.2007.04.013
77. Flasiński, M.; Hąc-Wydro, K. Natural vs synthetic auxin: Studies on the interactions between plant hormones and biological membrane lipids Environ. Res. 2014, 133, 123-134 10.1016/j.envres.2014.05.019
78. Martinoia, E.; Grill, E.; Tommasini, R.; Kreuz, K.; Amrhein, N. ATP-dependent glutathione S-conjugate export pump in the vacuolar membrane of plants Nature 1993, 364, 247-249 10.1038/364247a0
79. Huntscha, S.; Rodriguez Velosa, D. M.; Schroth, M. H.; Hollender, J. Degradation of polar organic micropollutants during riverbank filtration: Complementary results from spatiotemporal sampling and push-pull tests Environ. Sci. Technol. 2013, 47, 11512-11521 10.1021/es401802z
80. McLachlan, J. A. Environmental Signaling: What Embryos and Evolution Teach Us About Endocrine Disrupting Chemicals Endocr. Rev. 2001, 22, 319-341 10.1210/edrv.22.3.0432
81. Leopold, A.; Erwin, M.; Oh, J.; Browning, B. Phytoestrogens: adverse effects on reproduction in California quail Science 1976, 191, 98-100 10.1126/science.1246602
82. Ludwig-Müller, J. Indole-3-butyric acid in plant growth and development Plant Growth Regul. 2000, 32, 219-230 10.1023/A:1010746806891
83. Mihaljević, S.; Salopek-Sondi, B. Alanine conjugate of indole-3-butyric acid improves rooting of highbush blueberries Plant Soil Environ. 2012, 58 (5) 236-241