title: Multiscale digital Arabidopsis predicts individual organ and whole-organism growth.
abstract: Understanding how dynamic molecular networks affect whole-organism physiology, analogous to mapping genotype to phenotype, remains a key challenge in biology. Quantitative models that represent processes at multiple scales and link understanding from several research domains can help to tackle this problem. Such integrated models are more common in crop science and ecophysiology than in the research communities that elucidate molecular networks. Several laboratories have modeled particular aspects of growth in Arabidopsis thaliana, but it was unclear whether these existing models could productively be combined. We test this approach by constructing a multiscale model of Arabidopsis rosette growth. Four existing models were integrated with minimal parameter modification (leaf water content and one flowering parameter used measured data). The resulting framework model links genetic regulation and biochemical dynamics to events at the organ and whole-plant levels, helping to understand the combined effects of endogenous and environmental regulators on Arabidopsis growth. The framework model was validated and tested with metabolic, physiological, and biomass data from two laboratories, for five photoperiods, three accessions, and a transgenic line, highlighting the plasticity of plant growth strategies. The model was extended to include stochastic development. Model simulations gave insight into the developmental control of leaf production and provided a quantitative explanation for the pleiotropic developmental phenotype caused by overexpression of miR156, which was an open question. Modular, multiscale models, assembling knowledge from systems biology to ecophysiology, will help to understand and to engineer plant behavior from the genome to the field.
authors.affiliation: SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JD, United Kingdom;
authors.forename: Yin Hoon
authors.initials: YH
authors.lastname: Chew
authors.affiliation: Institut National de la Recherche Agronomique and Université Bordeaux, Unité Mixte de Recherche 1332 de Biologie du Fruit et Pathologie, F-33140 Villenave d'Ornon, France;
authors.forename: Bénédicte
authors.initials: B
authors.lastname: Wenden
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany;
authors.forename: Anna
authors.initials: A
authors.lastname: Flis
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany;
authors.forename: Virginie
authors.initials: V
authors.lastname: Mengin
authors.affiliation: Simulistics Ltd., Loanhead EH20 9PA, United Kingdom;
authors.forename: Jasper
authors.initials: J
authors.lastname: Taylor
authors.affiliation: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 2FG, United Kingdom;
authors.forename: Christopher L
authors.initials: CL
authors.lastname: Davey
authors.affiliation: SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JD, United Kingdom;
authors.forename: Christopher
authors.initials: C
authors.lastname: Tindal
authors.affiliation: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 2FG, United Kingdom;
authors.forename: Howard
authors.initials: H
authors.lastname: Thomas
authors.affiliation: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth SY23 2FG, United Kingdom;
authors.forename: Helen J
authors.initials: HJ
authors.lastname: Ougham
authors.affiliation: Cirad-Amis, Unité Mixte de Recherche, Association pour le Maintien d'une Agriculture Paysanne, F-34398 Montpellier Cedex 5, France; and.
authors.forename: Philippe
authors.initials: P
authors.lastname: de Reffye
authors.affiliation: Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany;
authors.forename: Mark
authors.initials: M
authors.lastname: Stitt
authors.affiliation: School of GeoSciences, University of Edinburgh, Edinburgh EH9 3JN, United Kingdom.
authors.forename: Mathew
authors.initials: M
authors.lastname: Williams
authors.affiliation: Simulistics Ltd., Loanhead EH20 9PA, United Kingdom;
authors.forename: Robert
authors.initials: R
authors.lastname: Muetzelfeldt
authors.affiliation: SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JD, United Kingdom;
authors.forename: Karen J
authors.initials: KJ
authors.lastname: Halliday
authors.affiliation: SynthSys and School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JD, United Kingdom; Andrew.Millar@ed.ac.uk.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Millar
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism; D002244:Carbon / Q000378:metabolism; D003198:Computer Simulation; D017753:Ecosystem; D017343:Genes, Plant; D053858:Metabolic Networks and Pathways; D008954:Models, Biological; D010641:Phenotype; D017440:Photoperiod; D010788:Photosynthesis; D018515:Plant Leaves / Q000254:growth & development; D030821:Plants, Genetically Modified; D013213:Starch / Q000378:metabolism; D013269:Stochastic Processes; D049490:Systems Biology
chemical_list: D002244:Carbon; D013213:Starch
keywords: crop modeling; digital organism; ecology; plant growth model