Transcriptional feedback regulation of YUCCA genes in response to auxin levels in Arabidopsis

Plant Cell Reports

Volumn 34, Issue 8, 2015, Pages 1343-1352

  Suzuki, Masashi ^a,b   Yamazaki, Chiaki ^a   Mitsui, Marie ^a   Kakei, Yusuke ^a   Mitani, Yuka ^a,b   Nakamura, Ayako ^a   Ishii, Takahiro ^c   Soeno, Kazuo ^c   Shimada, Yukihisa ^a,b  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c NATIONAL AGRICULTURAL RESEARCH CENTER FOR WESTERN REGION   (Japan)

Author keywords

Auxin biosynthesis; Auxin homeostasis; Indole 3 acetic acid; Indole 3 pyruvic acid; Transcriptional regulation; YUCCA

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

1-NAPHTHALENEACETIC ACID; 2,4 DICHLOROPHENOXYACETIC ACID; ARABIDOPSIS PROTEIN; ARYLACETIC ACID DERIVATIVE; INDOL-3-YL PYRUVIC ACID; INDOLE DERIVATIVE; INDOLEACETIC ACID DERIVATIVE; OXYGENASE; PHYTOHORMONE; YUC PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; DRUG EFFECTS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT GENE; SEEDLING;

2,4-DICHLOROPHENOXYACETIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INDOLEACETIC ACIDS; INDOLES; NAPHTHALENEACETIC ACIDS; OXYGENASES; PLANT GROWTH REGULATORS; SEEDLINGS;

EID: 84931567882     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-015-1791-z     Document Type: Article

References (65)

1. Abel S, Nguyen MD, Theologis A (1995) The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J Mol Biol 251:533–549
2. Boerjan W, Cervera M-T, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Onckelen HV, Montagu MV, Inzé D (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419
3. Brandt R, Salla-Martret M, Bou-Torrent J, Musielak T, Stahl M, Lanz C, Ott F, Schmid M, Greb T, Schwarz M, Choi S-B, Barton MK, Reinhart BJ, Liu T, Quint M, Palauqui J-C, Martínez-Gracía JF, Wenkel S (2012) Genome-wide binding-site analysis of REVOLUTA reveals a link between leaf patterning and light-mediated growth responses. Plant J 72:31–42
4. Cheng Y, Dai X, 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
5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
6. Cohen JD, Bandurski RS (1982) Chemistry and physiology of the bound auxins. Annu Rev Plant Physiol 33:403–430
7. Dai X, Mashiguchi K, Chen Q, Kasahara H, Kamiya Y, Ojha S, DuBois J, Ballou D, Zhao Y (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J Biol Chem 288:1448–1457
8. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song KM, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629
9. Eklund DM, Ståldal V, Valsecchi I, Cierlik I, Eriksson C, Hiratsu K, Ohme-Takagi M, Sundström JF, Thelander M, Ezcurra I, Sundberg E (2010) The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22:349–363
10. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, Ye S, Yu P, Breen G, Cohen JD, Wigge PA, Gray WM (2011) Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108:20231–20235
11. Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334
12. TIR1 auxin receptor complex. ACS Chem Biol 7:590–598
13. He W, Brumos J, Li H, Ji Y, Ke M, Gong X, Zeng Q, Li W, Zhang X, An F, Wen X, Li P, Chu J, Sun X, Yan C, Yan N, Xie D-Y, Raikhel N, Yang Z, Stepanova AN, Alonso JM, Guo H (2011) A small-molecule screen identifies l-kynurenine as a competitive inhibitor of TAA1/TAR activity in ethylene-directed auxin biosynthesis and root growth in Arabidopsis. Plant Cell 23:3944–3960
14. Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J, Pollmann S (2013) The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J 74:626–637
15. Higashide T, Narukawa M, Shimada Y, Soeno K (2014) Suppression of elongation and growth of tomato seedlings by auxin biosynthesis inhibitors and modeling of the growth and environmental response. Sci Rep 4:4556
16. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, López-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand S, Xenarios I, Fankhauser C (2012) Phytochrome interacting fators 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711
17. Ishida Y, Hayashi K, Soeno K, Asami T, Nakamura S, Suzuki M, Nakamura A, Shimada Y (2014) Analysis of a putative auxin biosynthesis inhibitor, indole-3-oxoethylphosphonic acid, in Arabidopsis. Biosci Biotechnol Biochem 78:67–70
18. Ishihara A, Hashimoto Y, Tanaka C, Dubouzet JG, Nakao T, Matsuda F, Nishioka T, Miyagawa H, Wakasa K (2008) The tryptophan pathway is involved in the defense responses of rice against pathogenic infection via serotonin production. Plant J 54:481–495
19. Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555
20. Kriechbaumer V, Wang P, Hawes C, Abell BM (2012) Alternative splicing of the auxin biosynthesis gene YUCCA4 determines its subcellular compartmentation. Plant J 70:292–302
21. Lee M, Jung J-H, Han D-Y, Seo PJ, Park WJ, Park C-M (2012) Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis. Planta 235:923–938
22. Lehmann T, Hoffmann M, Hentrich M, Pollmann S (2010) Indole-3-acetamide-dependent auxin biosynthesis: a widely distributed way of indole-3-acetic acid production? Eur J Cell Biol 89:895–905
23. Li L-C, Qin G-J, Tsuge T, Hou X-H, Ding M-Y, Aoyama T, Oka A, Chen Z, Gu H, Zhao Y, Qu L-J (2008) SPOROCYTELESS modulates YUCCA expression to regulate the development of lateral organs in Arabidopsis. New Phytol 179:751–764
24. Li L, Ljung K, Breton G, Schmitz RJ, Pruneda-Paz J, Cowing-Zitron C, Cole BJ, Ivans LJ, Pedmale UV, Jung H-S, Ecker JR, Kay SA, Chory J (2012) Linking photoreceptor excitation to changes in plant architecture. Genes Dev 26:785–790
25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta] CT methods. Methods 25:402–408
26. Ljung K (2013) Auxin metabolism and homeostasis during plant development. Development 140:943–950
27. Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J 28:465–474
28. Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J, Cohen JD, Sandberg G (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 50:309–332
29. Ludwig-Müller J (2011) Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot 62:1757–1773
30. Ma Q, Robert S (2014) Auxin biology revealed by small molecules. Physiol Plant 151:25–42
31. Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872
32. 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 (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108:18512–18517
33. Mori Y, Nishimura T, Koshiba T (2005) Vigorous synthesis of indole-3-acetic acid in the apical very tip leads to a constant basipetal flow of the hormone in maize coleoptiles. Plant Sci 168:467–473
34. Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853
35. Nemoto K, Hara M, Suzuki M, Seki H, Muranaka T, Mano Y (2009) The NtAMI1 gene functions in cell division of tobacco BY-2 cells in the presence of indole-3-acetamide. FEBS Lett 583:487–492
36. Nishimura T, Hayashi K, Suzuki H, Gyohda A, Takaoka C, Sakaguchi Y, Matsumoto S, Kasahara H, Sakai T, Kato J, Kamiya Y, Koshiba T (2014) Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis. Plant J 77:352–366
37. Pacheco-Villalobos D, Sankar M, Ljung K, Hardtke CS (2013) Disturbed local auxin homeostasis enhances cellular anisotropy and reveals alternative wiring of auxin-ethylene crosstalk in Brachypodium distachyon seminal roots. PLoS Genet 9:e1003564
38. Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110:1107–1112
39. Pollmann S, Neu D, Weiler EW (2003) Molecular cloning and characterization of an amidase from Arabidopsis thaliana capable of converting indole-3-acetamide into the plant growth hormone, indole-3-acetic acid. Phytochemistry 62:293–300
40. Quittenden LJ, Davies NW, Smith JA, Molesworth PP, Tivendale ND, Ross JJ (2009) Auxin biosynthesis in pea: characterization of the tryptamine pathway. Plant Physiol 151:1130–1138
41. Quittenden LJ, McAdam EL, Davies NW, Ross JJ (2014) Evidence that indole-3-acetic acid is not synthesized via the indole-3-acetamide pathway in pea roots. J Plant Growth Regul 33:831–836
42. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL (2009) REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 106:16883–16888
43. Rosquete MR, Barbez E, Kleine-Vehn J (2012) Cellular auxin homeostasis: gatekeeping is housekeeping. Mol Plant 5:772–786
44. Soeno K, Goda H, Ishii T, Ogura T, Tachikawa T, Sasaki E, Yoshida S, Fujioka S, Asami T, Shimada Y (2010) Auxin biosynthesis inhibitors, identified by a genomics-based approach, provide insights into auxin biosynthesis. Plant Cell Physiol 51:524–536
45. Sohlberg JJ, Myrenås M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E (2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of Arabidopsis gynoecium. Plant J 47:112–123
46. Spiess GM, Hausman A, Yu P, Cohen JD, Rampey RA, Zolman BK (2014) Auxin input pathway distributions are mitigated by changes in auxin biosynthetic gene expression in Arabidopsis. Plant Physiol 165:1092–1104
47. Ståldal V, Cierlik I, Chen S, Landberg K, Baylis T, Myrenås M, Sundström JF, Eklund DM, Ljung K, Sundberg E (2012) The Arabidopsis thaliana transcriptional activator STYLISH1 regulates genes affecting stamen development, cell expansion and timing of flowering. Plant Mol Biol 78:545–559
48. Staswick PE (2009) The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol 150:1310–1321
49. Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie D-Y, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191
50. Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23:3961–3973
51. Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh T-F, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDONE2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA 105:3151–3156
52. Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Zhao Y, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 106:5430–5435
53. Sun J, Qi L, Li Y, Chu J, Li C (2012) PIF4-mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet 8:e1002594
54. Tao Y, Ferrer J-L, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballaré CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176
55. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859
56. Tivendale ND, Davis NW, Molesworth PP, Davidson SE, Smith JA, Lowe EK, Reid JB, Ross JJ (2010) Reassessing the role of N-hydroxytryptamine in auxin biosynthesis. Plant Physiol 154:1957–1965
57. Tivendale ND, Ross JJ, Cohen JD (2014) The shifting paradigms of auxin biosynthesis. Trends Plant Sci 19:44–51
58. Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (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. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
60. Yamada M, Greenham K, Prigge MJ, Jensen PJ, Estelle M (2009) The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol 151:168–179
61. Zhao Y (2012) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338
62. Zhao Y (2014) Auxin biosynthesis. Arabidopsis book 12:e0173
63. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309
64. Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvment of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112
65. Zheng Z, Guo Y, Novák O, Dai X, Zhao Y, Ljung K, Noel JP, Chory J (2013) Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol 9:244–248