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Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis.
Proc Natl Acad Sci U S A. 2016 09 27; 113(39):11022-7.PN

Abstract

The hormone auxin is a key regulator of plant growth and development, and great progress has been made understanding auxin transport and signaling. Here, we show that auxin metabolism and homeostasis are also regulated in a complex manner. The principal auxin degradation pathways in Arabidopsis include oxidation by Arabidopsis thaliana gene DIOXYGENASE FOR AUXIN OXIDATION 1/2 (AtDAO1/2) and conjugation by Gretchen Hagen3s (GH3s). Metabolic profiling of dao1-1 root tissues revealed a 50% decrease in the oxidation product 2-oxoindole-3-acetic acid (oxIAA) and increases in the conjugated forms indole-3-acetic acid aspartic acid (IAA-Asp) and indole-3-acetic acid glutamic acid (IAA-Glu) of 438- and 240-fold, respectively, whereas auxin remains close to the WT. By fitting parameter values to a mathematical model of these metabolic pathways, we show that, in addition to reduced oxidation, both auxin biosynthesis and conjugation are increased in dao1-1 Transcripts of AtDAO1 and GH3 genes increase in response to auxin over different timescales and concentration ranges. Including this regulation of AtDAO1 and GH3 in an extended model reveals that auxin oxidation is more important for auxin homoeostasis at lower hormone concentrations, whereas auxin conjugation is most significant at high auxin levels. Finally, embedding our homeostasis model in a multicellular simulation to assess the spatial effect of the dao1-1 mutant shows that auxin increases in outer root tissues in agreement with the dao1-1 mutant root hair phenotype. We conclude that auxin homeostasis is dependent on AtDAO1, acting in concert with GH3, to maintain auxin at optimal levels for plant growth and development.

Authors+Show Affiliations

Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom;Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Plant Sciences, School of Biology, Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom;Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom; malcolm.bennett@nottingham.ac.uk Markus.Owen@nottingham.ac.uk.Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom; Centre for Mathematical Medicine and Biology, School of Mathematical Sciences, University of Nottingham, Nottingham NG7 2RD, United Kingdom; malcolm.bennett@nottingham.ac.uk Markus.Owen@nottingham.ac.uk.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27651495

Citation

Mellor, Nathan, et al. "Dynamic Regulation of Auxin Oxidase and Conjugating Enzymes AtDAO1 and GH3 Modulates Auxin Homeostasis." Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 39, 2016, pp. 11022-7.
Mellor N, Band LR, Pěnčík A, et al. Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc Natl Acad Sci U S A. 2016;113(39):11022-7.
Mellor, N., Band, L. R., Pěnčík, A., Novák, O., Rashed, A., Holman, T., Wilson, M. H., Voβ, U., Bishopp, A., King, J. R., Ljung, K., Bennett, M. J., & Owen, M. R. (2016). Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proceedings of the National Academy of Sciences of the United States of America, 113(39), 11022-7. https://doi.org/10.1073/pnas.1604458113
Mellor N, et al. Dynamic Regulation of Auxin Oxidase and Conjugating Enzymes AtDAO1 and GH3 Modulates Auxin Homeostasis. Proc Natl Acad Sci U S A. 2016 09 27;113(39):11022-7. PubMed PMID: 27651495.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. AU - Mellor,Nathan, AU - Band,Leah R, AU - Pěnčík,Aleš, AU - Novák,Ondřej, AU - Rashed,Afaf, AU - Holman,Tara, AU - Wilson,Michael H, AU - Voβ,Ute, AU - Bishopp,Anthony, AU - King,John R, AU - Ljung,Karin, AU - Bennett,Malcolm J, AU - Owen,Markus R, Y1 - 2016/09/20/ PY - 2016/9/22/entrez PY - 2016/9/22/pubmed PY - 2018/1/27/medline KW - Arabidopsis thaliana KW - auxin KW - homeostasis KW - hormone regulation KW - metabolism SP - 11022 EP - 7 JF - Proceedings of the National Academy of Sciences of the United States of America JO - Proc Natl Acad Sci U S A VL - 113 IS - 39 N2 - The hormone auxin is a key regulator of plant growth and development, and great progress has been made understanding auxin transport and signaling. Here, we show that auxin metabolism and homeostasis are also regulated in a complex manner. The principal auxin degradation pathways in Arabidopsis include oxidation by Arabidopsis thaliana gene DIOXYGENASE FOR AUXIN OXIDATION 1/2 (AtDAO1/2) and conjugation by Gretchen Hagen3s (GH3s). Metabolic profiling of dao1-1 root tissues revealed a 50% decrease in the oxidation product 2-oxoindole-3-acetic acid (oxIAA) and increases in the conjugated forms indole-3-acetic acid aspartic acid (IAA-Asp) and indole-3-acetic acid glutamic acid (IAA-Glu) of 438- and 240-fold, respectively, whereas auxin remains close to the WT. By fitting parameter values to a mathematical model of these metabolic pathways, we show that, in addition to reduced oxidation, both auxin biosynthesis and conjugation are increased in dao1-1 Transcripts of AtDAO1 and GH3 genes increase in response to auxin over different timescales and concentration ranges. Including this regulation of AtDAO1 and GH3 in an extended model reveals that auxin oxidation is more important for auxin homoeostasis at lower hormone concentrations, whereas auxin conjugation is most significant at high auxin levels. Finally, embedding our homeostasis model in a multicellular simulation to assess the spatial effect of the dao1-1 mutant shows that auxin increases in outer root tissues in agreement with the dao1-1 mutant root hair phenotype. We conclude that auxin homeostasis is dependent on AtDAO1, acting in concert with GH3, to maintain auxin at optimal levels for plant growth and development. SN - 1091-6490 UR - https://www.unboundmedicine.com/medline/citation/27651495/Dynamic_regulation_of_auxin_oxidase_and_conjugating_enzymes_AtDAO1_and_GH3_modulates_auxin_homeostasis_ L2 - https://www.pnas.org/doi/10.1073/pnas.1604458113?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -