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Overexpression of the bacterial tryptophan oxidase RebO affects auxin biosynthesis and Arabidopsis development

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  • Life & Medical Sciences
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Science Bulletin

Abstract

Both tryptophan (Trp) and auxin are essential for plant growth and Trp is a precursor for auxin biosynthesis. Concentrations of Trp and auxin need to be tightly controlled to ensure optimal growth and development. It has been very difficult to study the homeostasis of these two essential and inter-dependent compounds. Auxin is mainly synthesized from Trp via a two-step pathway using indole-3-pyruvate (IPA) as the intermediate. Here we used a bacterial Trp oxidase RebO, which does not exist in Arabidopsis and which converts Trp to the imine form of IPA, to modulate IPA levels in Arabidopsis. Our results demonstrate that Arabidopsis plants use two strategies to ensure that no excess IPA is made from Trp. IPA is made from Trp by the TAA family of aminotransferases, which we show catalyzes the reverse reaction when IPA level is high. Moreover, excess IPA is converted back to Trp by the VAS1 aminotransferase. We show that the VAS1-catalyzed reaction is very important for Trp homeostasis. This work not only elucidates the intricate biochemical mechanisms that control the homeostasis of Trp, IPA, and auxin, but also provides novel tools for further biochemical studies on Trp metabolism and auxin biosynthesis in plants.

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References

  1. Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  Google Scholar 

  2. Zhao Y (2014) Auxin biosynthesis. The Arabidopsis book 12:e0173

  3. 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

    Article  Google Scholar 

  4. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    Article  Google Scholar 

  5. Pinon V, Prasad K, Grigg SP et al (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110:1107–1112

    Article  Google Scholar 

  6. Stepanova AN, Robertson-Hoyt J, Yun J et al (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191

    Article  Google Scholar 

  7. Tao Y, Ferrer JL, Ljung K et al (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133:164–176

    Article  Google Scholar 

  8. Won C, Shen X, Mashiguchi K 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

    Article  Google Scholar 

  9. Dai X, Mashiguchi K, Chen Q et al (2013) The biochemical mechanism of auxin biosynthesis by an Arabidopsis YUCCA flavin-containing monooxygenase. J Biol Chem 288:1448–1457

    Article  Google Scholar 

  10. Mashiguchi K, Tanaka K, Sakai T et al (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci USA 108:18512–18517

    Article  Google Scholar 

  11. Phillips KA, Skirpan AL, Liu X et al (2011) vanishing tassel2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23:550–566

    Article  Google Scholar 

  12. Stepanova AN, Yun J, Robles LM et al (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23:3961–3973

    Article  Google Scholar 

  13. Zhao Y, Hull AK, Gupta NR et al (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450 s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112

    Article  Google Scholar 

  14. Zhao Y, Christensen SK, Fankhauser C et al (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309

    Article  Google Scholar 

  15. Pedmale UV, Huang SS, Zander M et al (2016) Cryptochromes interact directly with PIFs to control plant growth in limiting blue light. Cell 164:233–245

    Article  Google Scholar 

  16. Zheng Z, Guo Y, Novak O et al (2013) Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol 9:244–246

    Article  Google Scholar 

  17. Nishizawa T, Aldrich CC, Sherman DH (2005) Molecular analysis of the rebeccamycin l-amino acid oxidase from Lechevalieria aerocolonigenes ATCC 39243. J Bacteriol 187:2084–2092

    Article  Google Scholar 

  18. Onaka H, Taniguchi S, Igarashi Y et al (2003) Characterization of the biosynthetic gene cluster of rebeccamycin from Lechevalieria aerocolonigenes ATCC 39243. Biosci Biotechnol Biochem 67:127–138

    Article  Google Scholar 

  19. Howard-Jones AR, Walsh CT (2005) Enzymatic generation of the chromopyrrolic acid scaffold of rebeccamycin by the tandem action of RebO and RebD. Biochemistry 44:15652–15663

    Article  Google Scholar 

  20. Sugawara S, Hishiyama S, Jikumaru Y et al (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 106:5430–5435

    Article  Google Scholar 

  21. Hobbie L, Estelle M (1994) Genetic approaches to auxin action. Plant, Cell Environ 17:525–540

    Article  Google Scholar 

  22. Yamada M, Greenham K, Prigge MJ et al (2009) The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol 151:168–179

    Article  Google Scholar 

  23. Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:921–934

    Article  Google Scholar 

  24. Boerjan W, Cervera MT, Delarue M et al (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419

    Article  Google Scholar 

  25. Delarue M, Prinsen E, Onckelen HV et al (1998) Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J 14:603–611

    Article  Google Scholar 

  26. He W, Brumos J, Li H et al (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

    Article  Google Scholar 

  27. Romano CP, Robson PR, Smith H et al (1995) Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants. Plant Mol Biol 27:1071–1083

    Article  Google Scholar 

  28. Pacheco-Villalobos D, Sankar M, Ljung K et al (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

    Article  Google Scholar 

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Acknowledgement

This work was supported by the NIH (R01GM114660 to YZ). ZZ and JC are supported by NIH (GM52413 to JC) and HHMI. JC is a HHMI investigator.

Author contributions

YZ and DB conceived the research. YG, XD, and YZ designed the experiments. YG and XD conducted the overexpression of RebO and analyzed the results. YK and HK did the auxin analysis. JC and ZZ conducted the shade avoidance assay. YZ wrote the paper.

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Correspondence to Yunde Zhao.

Additional information

Yangbin Gao and Xinhua Dai contributed equally to this work.

SPECIAL TOPIC: Plant Development and Reproduction.

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Gao, Y., Dai, X., Zheng, Z. et al. Overexpression of the bacterial tryptophan oxidase RebO affects auxin biosynthesis and Arabidopsis development. Sci. Bull. 61, 859–867 (2016). https://doi.org/10.1007/s11434-016-1066-2

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  • DOI: https://doi.org/10.1007/s11434-016-1066-2

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