title: SIZ1-Dependent Post-Translational Modification by SUMO Modulates Sugar Signaling and Metabolism in Arabidopsis thaliana.
abstract: Post-translational modification mechanisms function as switches that mediate the balance between optimum growth and the response to environmental stimuli, by regulating the activity of key proteins. SUMO (small ubiquitin-like modifier) attachment, or sumoylation, is a post-translational modification that is essential for the plant stress response, also modulating hormonal circuits to co-ordinate developmental processes. The Arabidopsis SUMO E3 ligase SAP and Miz 1 (SIZ1) is the major SUMO conjugation enhancer in response to stress, and is implicated in several aspects of plant development. Here we report that known SUMO targets are over-represented in multiple carbohydrate-related proteins, suggesting a functional link between sumoylation and sugar metabolism and signaling in plants. We subsequently observed that SUMO-conjugated proteins accumulate in response to high doses of sugar in a SIZ1-dependent manner, and that the null siz1 mutant displays increased expression of sucrose and starch catabolic genes and shows reduced starch levels. We demonstrated that SIZ1 controls germination time and post-germination growth via osmotic and sugar-dependent signaling, respectively. Glucose was specifically linked to SUMO-sugar interplay, with high levels inducing root growth inhibition and aberrant root hair morphology in siz1. The use of sugar analogs and sugar marker gene expression analysis allowed us to implicate SIZ1 in a signaling pathway dependent on glucose metabolism, probably involving modulation of SNF1-related kinase 1 (SnRK1) activity.
authors.affiliation: BioSystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal These authors contributed equally to this work.
authors.forename: Pedro Humberto
authors.initials: PH
authors.lastname: Castro
authors.affiliation: BioSystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal CIBIO, InBIO-Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal These authors contributed equally to this work.
authors.forename: Nuno
authors.initials: N
authors.lastname: Verde
authors.affiliation: BioSystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal CIBIO, InBIO-Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.
authors.forename: Tiago
authors.initials: T
authors.lastname: Lourenço
authors.affiliation: BioSystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal CIBIO, InBIO-Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal.
authors.forename: Alexandre Papadopoulos
authors.initials: AP
authors.lastname: Magalhães
authors.affiliation: BioSystems & Integrative Sciences Institute (BioISI), Plant Functional Biology Center, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal.
authors.forename: Rui Manuel
authors.initials: RM
authors.lastname: Tavares
authors.affiliation: Instituto de Hortofruticultura Subtropical y Mediterránea 'La Mayora', Universidad de Málaga-Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Departamento de Biología Celular, Genética y Fisiología, Universidad de Málaga, Campus Teatinos, 29071 Málaga, Spain.
authors.forename: Eduardo Rodríguez
authors.initials: ER
authors.lastname: Bejarano
authors.affiliation: CIBIO, InBIO-Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal hazevedo@cibio.up.pt.
authors.forename: Herlânder
authors.initials: H
authors.lastname: Azevedo
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D050260:Carbohydrate Metabolism / Q000187:drug effects / Q000235:genetics; D002241:Carbohydrates / Q000494:pharmacology; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D017343:Genes, Plant; D018525:Germination / Q000187:drug effects / Q000235:genetics; D005947:Glucose / Q000494:pharmacology; D006593:Hexokinase / Q000378:metabolism; D008025:Ligases / Q000235:genetics / Q000378:metabolism*; D008954:Models, Biological; D008970:Molecular Weight; D009154:Mutation / Q000235:genetics; D010641:Phenotype; D018517:Plant Roots / Q000033:anatomy & histology / Q000187:drug effects / Q000254:growth & development; D011499:Protein Processing, Post-Translational / Q000187:drug effects / Q000235:genetics; D017346:Protein Serine-Threonine Kinases / Q000378:metabolism; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects / Q000235:genetics; D025841:Small Ubiquitin-Related Modifier Proteins / Q000378:metabolism*; D013213:Starch / Q000378:metabolism; D013395:Sucrose / Q000378:metabolism; D058207:Sumoylation
chemical_list: D029681:Arabidopsis Proteins; D002241:Carbohydrates; D005947:Glucose; D006593:Hexokinase; D008025:Ligases; D017346:Protein Serine-Threonine Kinases; D012333:RNA, Messenger; D025841:Small Ubiquitin-Related Modifier Proteins; D013213:Starch; D013395:Sucrose; C531469:At3g01090 protein, Arabidopsis; C502552:SIZ1 protein, Arabidopsis
keywords: 2-Deoxyglucose; Arabidopsis; Glucose; Post-germination growth arrest; SIZ1; SUMO