Distinct Characteristics of Indole-3-Acetic Acid and Phenylacetic Acid, Two Common Auxins in Plants

Plant and Cell Physiology

Volumn 56, Issue 8, 2015, Pages 1641-1654

  Sugawara, Satoko ^a   Mashiguchi, Kiyoshi ^a   Tanaka, Keita ^a,b   Hishiyama, Shojiro ^c   Sakai, Tatsuya ^d   Hanada, Kousuke ^e   Kinoshita Tsujimura, Kaori ^f   Yu, Hong ^g   Dai, Xinhua ^g   Takebayashi, Yumiko ^a   Takeda Kamiya, Noriko ^a   Kakimoto, Tatsuo ^f   Kawaide, Hiroshi ^b   Natsume, Masahiro ^b   Estelle, Mark ^g   Zhao, Yunde ^g   Hayashi, Ken Ichiro ^h   Kamiya, Yuji ^a   Kasahara, Hiroyuki ^a,i  

^a RIKEN Plant Science Center   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c FORESTRY AND FOREST PRODUCTS RESEARCH INSTITUTE   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

^e KYUSHU INSTITUTE OF TECHNOLOGY   (Japan)

^f OSAKA UNIVERSITY   (Japan)

^g SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^h OKAYAMA UNIVERSITY OF SCIENCE   (Japan)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Auxin transport; Indole 3 acetic acid; Metabolism; Phenylacetic acid; Signal transduction

Indexed keywords

ARABIDOPSIS; TRACHEOPHYTA; ZEA MAYS;

ARABIDOPSIS PROTEIN; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; OXYGENASE; PHENYLACETIC ACID; PHENYLACETIC ACID DERIVATIVE; PHYTOHORMONE; YUC PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLISM; REPORTER GENE; SIGNAL TRANSDUCTION; TRANSGENIC PLANT; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; INDOLEACETIC ACIDS; OXYGENASES; PHENYLACETATES; PLANT GROWTH REGULATORS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION; ZEA MAYS;

EID: 84939512569     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv088     Document Type: Article

References (64)

1. Bak, S., Nielsen, H.L. and Halkier, B.A. (1998) The presence of CYP79 homologues in glucosinolate-producing plants shows evolutionary conservation of the enzymes in the conversion of amino acid to aldoxime in the biosynthesis of cyanogenic glucosides and glucosinolates. Plant Mol. Biol. 38: 725-734.
2. Barbez, E., Kubes, M., Rolcik, J., Béziat, C., Penćk, A., Wang, B., et al. (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 485: 119-122.
3. Beyer, E.M. (1972) Auxin transport: a new synthetic inhibitor. Plant Physiol. 50: 322-327.
4. Brumos, J., Alonso, J.M. and Stepanova, A.N. (2014) Genetic aspects of auxin biosynthesis and its regulation. Physiol. Plant. 151: 3-12.
5. Calderon Villalobos, L.I., Lee, S., De Oliveira, C., Ivetac, A., Brandt, W., Armitage, L., et al. (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat. Chem. Biol. 8: 477-485.
6. Calderon-Villalobos, L.I., Tan, X., Zheng, N. and Estelle, M. (2010) Auxin perception-structural insights. Cold Spring Harb. Perspect. Biol. 2: a005546.
7. Chen, Q., Dai, X., De-Paoli, H., Cheng, Y., Takebayashi, Y., Kasahara, H., et al. (2014) Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55: 1072-1079.
8. Cheng, Y., Dai, X. and Zhao, Y. (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev. 20: 1790-1799.
9. Dai, X., Mashiguchi, K., Chen, Q., Kasahara, H., Kamiya, Y., Ojha, S., et al. (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J. Biol. Chem. 288: 1448-1457.
10. Davies, P.J. (2004) The plant hormones: their nature, occurrence, and functions. In Plant Hormones-Biosynthesis, Signal Transduction, Action! Edited by Davies, P.J. pp. 1-15. Kluwer Academic Publishers, Dordrecht.
11. Delbarre, A., Muller, P., Imhoff, V. and Guern, J. (1996) Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198: 532-541.
12. Dharmasiri, N., Dharmasiri, S. and Estelle, M. (2005) The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
13. Friml, J. (2010) Subcellular trafficking of PIN auxin efflux carriers in auxin transport. Eur. J. Cell Biol. 89: 231-235.
14. Gallavotti, A., Barazesh, S., Malcomber, S., Hall, D., Jackson, D., Schmidt, R.J., et al. (2008) sparse inflorescence1 encodes a monocot-specific YUCCAlike gene required for vegetative and reproductive development in maize. Proc. Natl Acad. Sci. USA 105: 15196-15201.
15. Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y. and Yoshida, S. (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 134: 1555-1573.
16. Haagen Smit, A.J. and Went, F.W. (1935) A physiological analysis of the growth substance. Proc. R. Acad. Amsterdam 38: 852-857.
17. Hayashi, K., Neve, J., Hirose, M., Kuboki, A., Shimada, Y., Kepinski, S., et al. (2012) Rational design of an auxin antagonist of the SCF(TIR1) auxin receptor complex. ACS Chem. Biol. 7: 590-598.
18. Hayashi, K., Tan, X., Zheng, N., Hatate, T., Kimura, Y., Kepinski, S., et al. (2008) Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc. Natl Acad Sci. USA 105: 5632-5637.
19. Hull, A.K., Vij, R. and Celenza, J.L. (2000) Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc. Natl Acad. Sci. USA 97: 2379-2384.
20. Jackson, R.G., Kowalczyk, M., Li, Y., Higgins, G., Ross, J., Sandberg, G., et al. (2002) Over-expression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterisation of transgenic lines. Plant J. 32: 573-583.
21. Jacobs, W.P., McCready, C.C. and Osborne, D.J. (1966) Transport of the auxin 2,4-dichlorophenoxyacetic acid through absiccion zones, pulvini, and petioles of Phaseolus vulgaris. Plant Physiol. 41: 725-730.
22. Kepinski, S. and Leyser, O. (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
23. Khan, S. and Stone, J.M. (2007) Arabidopsis thaliana GH3.9 influences primary root growth. Planta 226: 21-34.
24. Korasick, D.A., Enders, T.A. and Strader, L.C. (2013) Auxin biosynthesis and storage forms. J. Exp. Bot. 64: 2541-2555
25. Kubes, M., Yang, H., Richter, G.L., Cheng, Y., M-l odzińska, E., Wang, X., et al. (2012) The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J. 69: 640-654.
26. Ljung, K., Bhalerao, R.P. and Sandberg, G. (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J. 28: 465-474.
27. Löbler, M. and Klämbt, D. (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.). I. Purification by immunological methods and characterization. J. Biol. Chem. 260: 9848-9853.
28. Ludwig-Müller, J. and Cohen, J.D. (2002) Identification and quantification of three active auxins in different tissues of Tropaeolum majus. Physiol. Plant. 115: 320-329.
29. Mashiguchi, K., Tanaka, K., Sakai, T., Sugawara, S., Kawaide, H., Natsume, M., et al. (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108: 18512-18517.
30. Mikkelsen, M.D., Hansen, C.H., Wittstock, U. and Halkier, B.A. (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J. Biol. Chem. 275: 33712-33717.
31. Morris, D.A. and Johnson, C.F. (1987) Regulation of auxin transport in pea (Pisum sativum L.) by phenylacetic acid: inhibition of polar auxin transport in intact plants and stem segments. Planta 172: 408-416.
32. Muir, R.M., Fujita, T. and Hansch, C. (1967) Structure-activity relationship in the auxin activity of mono-substituted phenylacetic acids. Plant Physiol. 42: 1519-1526.
33. Nemhauser, J.L., Hong, F. and Chory, J. (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126: 467-475.
34. Nishimura, T., Nakano, H., Hayashi, K., Niwa, C. and Koshiba, T. (2009) Differential downward stream of auxin synthesized at the tip has a key role in gravitropic curvature via TIR1/AFBs-mediated auxin signaling pathways. Plant Cell Physiol. 50: 1874-1885.
35. Nishiyama, T., Hiwatashi, Y., Sakakibara, I., Kato, M. and Hasebe, M. (2000) Tagged mutagenesis and gene-trap in the moss, Physcomitrella patens by shuttle mutagenesis. DNA Res. 7: 9-17.
36. Parry, G., Calderon-Villalobos, L.I., Prigge, M., Peret, B., Dharmasiri, S., Itoh, H., et al. (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc. Natl Acad. Sci. USA 106: 22540-22545.
37. Penćk, A., Simonovik, B., Petersson, S.V., Henyková, E., Simon, S., Greenham, K., et al. (2013) Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell, 25:3858-3870.
38. Petrasek, J., Mravec, J., Bouchard, R., Blakeslee, J.J., Abas, M., Seifertova, D., et al. (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918.
39. Phillips, K.A., Skirpan, A.L., Liu, X., Christensen, A., Slewinski, T.L., Hudson, C., et al. (2011) vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23: 550-566.
40. Procházka, S. and Borkovec, V. (1984) Transport and regulative properties of phenylacetic acid. Biol. Plant. 26: 358-363.
41. Qin, G., Gu, H., Zhao, Y., Ma, Z., Shi, G., Yang, Y., et al. (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17: 2693-2704.
42. Schneider, E.A., Kazakoff, C.W. and Wightman, F. (1985) Gas chromatography-mass spectrometry evidence for several endogenous auxins in pea seedling organs. Planta 165: 232-241.
43. Shimizu-Mitao, Y. and Kakimoto, T. (2014) Auxin sensitivities of all Arabidopsis Aux/IAAs for degradation in the presence of every TIR1/AFB. Plant Cell Physiol. 55: 1450-1459.
44. Simon, S. and Petrasek, J. (2011) Why plants need more than one type of auxin. Plant Sci. 180: 454-460.
45. Small, D.K. and Morris, D.A. (1990) Promotion of elongation and acid invertase activity in Phaseolus vulgaris L. internode segments by phenylacetic acid. Plant Growth Regul. 9: 329-340.
46. Smyth, G.K., Michaud, J. and Scott, H.S. (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075.
47. Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M.T., Maldonado, M.C., et al. (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17: 616-627.
48. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.Y., Dolezal, K., et al. (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177-191.
49. Stepanova, A.N., Yun, J., Robles, L.M., Novak, O., He, W., Guo, H., et al. (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23: 3961-3973.
50. Sugawara, S., Hishiyama, S., Jikumaru, Y., Hanada, A., Nishimura, T., Koshiba, T., et al. (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc. Natl Acad. Sci. USA 106: 5430-5435.
51. Suttle, J.C. and Mansager, E.R. (1986) The physiological significance of phenylacetic acid in abscising cotton cotyledons. Plant Physiol. 81: 434-438.
52. Swarup R. Peret B. (2012) AUX/LAX family of auxin influx carriers-an overview. Front. Plant Sci, 3:225.
53. Tanaka, K., Hayashi, K., Natsume, M., Kamiya, Y., Sakakibara, H., Kawaide, H., et al. (2014) UGT74D1 catalyzes the glucosylation of 2-oxindole-3-acetic acid in the auxin metabolic pathway in Arabidopsis. Plant Cell Physiol. 55: 218-228.
54. Tao, Y., Ferrer, J.L., Ljung, K., Pojer, F., Hong, F., Long, J.A., et al. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133: 164-176.
55. Van Overbeek, J. (1959) Auxins. Bot. Rev. 25: 269-350.
56. Wightman, F. and Lighty, D.L. (1982) Identification of phenylacetic acid as natural auxin in the shoots of higher plants. Physiol. Plant. 55: 17-24.
57. Wittstock, U. and Halkier, B.A. (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. catalyzes the conversion of l-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J. Biol. Chem. 275: 14659-14666.
58. Won, C., Shen, X., Mashiguchi, K., Zheng, Z., Dai, X., Cheng, Y., et al. (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc. Natl Acad. Sci. USA 108: 18518-18523.
59. Yamamoto, M. and Yamamoto, K.T. (1998) Differential effects of 1-naphthaleneacetic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid on the gravitropic response of roots in an auxin-resistant mutant of arabidopsis, aux1. Plant Cell Physiol. 39: 660-664.
60. Yang, Y., Hammes, U.Z., Taylor, C.G., Schachtman, D.P. and Nielsen, E. (2006) High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16: 1123-1127.
61. Yu, H., Moss, B.L., Jang, S.S., Prigge, M., Klavins, E., Nemhauser, J.L., et al. (2013) Mutations in the TIR1 auxin receptor that increase affinity for auxin/indole-3-acetic acid proteins result in auxin hypersensitivity. Plant Physiol. 162: 295-303.
62. Zhao, Y. (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol. Plant 5: 334-338.
63. Zhao, Y., Christensen, S.K., Fankhauser, C., Cashman, J.R., Cohen, J.D., Weigel, D., et al. (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291: 306-309.
64. Zhao, Z., Zhang, Y., Liu, X., Zhang, X., Liu, S., Yu, X., et al. (2013) A role for a dioxygenase in auxin metabolism and reproductive development in rice. Dev Cell 27: 113-122.