title: Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis.
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.affiliation: 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;
authors.forename: Nathan
authors.initials: N
authors.lastname: Mellor
authors.affiliation: 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;
authors.forename: Leah R
authors.initials: LR
authors.lastname: Band
authors.affiliation: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;
authors.forename: Aleš
authors.initials: A
authors.lastname: Pěnčík
authors.affiliation: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;
authors.forename: Ondřej
authors.identifier: 0000-0003-3452-0154
authors.initials: O
authors.lastname: Novák
authors.affiliation: Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;
authors.forename: Afaf
authors.initials: A
authors.lastname: Rashed
authors.affiliation: Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;
authors.forename: Tara
authors.initials: T
authors.lastname: Holman
authors.affiliation: 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.
authors.forename: Michael H
authors.initials: MH
authors.lastname: Wilson
authors.affiliation: Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;
authors.forename: Ute
authors.initials: U
authors.lastname: Voß
authors.affiliation: Centre for Plant Integrative Biology, Division of Plant and Crop Sciences, School of Biosciences, University of Nottingham, Loughborough LE12 5RD, United Kingdom;
authors.forename: Anthony
authors.initials: A
authors.lastname: Bishopp
authors.affiliation: 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;
authors.forename: John R
authors.initials: JR
authors.lastname: King
authors.affiliation: Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, SE-901 83 Umea, Sweden;
authors.forename: Karin
authors.identifier: 0000-0003-2901-189X
authors.initials: K
authors.lastname: Ljung
authors.affiliation: 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.
authors.forename: Malcolm J
authors.identifier: 0000-0003-0475-390X
authors.initials: MJ
authors.lastname: Bennett
authors.affiliation: 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.
authors.forename: Markus R
authors.identifier: 0000-0002-3028-9138
authors.initials: MR
authors.lastname: Owen
mesh_terms: D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D003198:Computer Simulation; D018506:Gene Expression Regulation, Plant; D006706:Homeostasis; D007210:Indoleacetic Acids / Q000378:metabolism*; D008954:Models, Biological; D009154:Mutation / Q000235:genetics; D010084:Oxidation-Reduction; D010088:Oxidoreductases / Q000378:metabolism*; D019441:Plant Epidermis / Q000378:metabolism; D018517:Plant Roots / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D014158:Transcription, Genetic
chemical_list: D029681:Arabidopsis Proteins; D007210:Indoleacetic Acids; D012333:RNA, Messenger; D010088:Oxidoreductases
keywords: Arabidopsis thaliana; auxin; homeostasis; hormone regulation; metabolism