title: Chloroplasts Are Central Players in Sugar-Induced Leaf Growth.
abstract: Leaves are the plant's powerhouses, providing energy for all organs through sugar production during photosynthesis. However, sugars serve not only as a metabolic energy source for sink tissues but also as signaling molecules, affecting gene expression through conserved signaling pathways to regulate plant growth and development. Here, we describe an in vitro experimental assay, allowing one to alter the sucrose (Suc) availability during early Arabidopsis (Arabidopsis thaliana) leaf development, with the aim to identify the affected cellular and molecular processes. The transfer of seedlings to Suc-containing medium showed a profound effect on leaf growth by stimulating cell proliferation and postponing the transition to cell expansion. Furthermore, rapidly after transfer to Suc, mesophyll cells contained fewer and smaller plastids, which are irregular in shape and contain fewer starch granules compared with control mesophyll cells. Short-term transcriptional responses after transfer to Suc revealed the repression of well-known sugar-responsive genes and multiple genes encoded by the plastid, on the one hand, and up-regulation of a GLUCOSE-6-PHOSPHATE TRANSPORTER (GPT2), on the other hand. Mutant gpt2 seedlings showed no stimulation of cell proliferation and no repression of chloroplast-encoded transcripts when transferred to Suc, suggesting that GPT2 plays a critical role in the Suc-mediated effects on early leaf growth. Our findings, therefore, suggest that induction of GPT2 expression by Suc increases the import of glucose-6-phosphate into the plastids that would repress chloroplast-encoded transcripts, restricting chloroplast differentiation. Retrograde signaling from the plastids would then delay the transition to cell expansion and stimulate cell proliferation.
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Judith
authors.identifier: 0000-0001-7887-6000
authors.initials: J
authors.lastname: Van Dingenen
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Liesbeth
authors.initials: L
authors.lastname: De Milde
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Mattias
authors.identifier: 0000-0003-4173-2366
authors.initials: M
authors.lastname: Vermeersch
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Katrien
authors.initials: K
authors.lastname: Maleux
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Riet
authors.identifier: 0000-0001-8270-7015
authors.initials: R
authors.lastname: De Rycke
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Michiel
authors.identifier: 0000-0002-1276-1857
authors.initials: M
authors.lastname: De Bruyne
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Véronique
authors.identifier: 0000-0003-4762-6580
authors.initials: V
authors.lastname: Storme
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Nathalie
authors.identifier: 0000-0002-3946-1758
authors.initials: N
authors.lastname: Gonzalez
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.).
authors.forename: Stijn
authors.identifier: 0000-0003-4402-2191
authors.initials: S
authors.lastname: Dhondt
authors.affiliation: Department of Plant Systems Biology, Vlaams Instituut voor Biotechnologie, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.); andDepartment of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium (J.V.D., L.D.M., M.V., K.M., R.D.R., M.D.B., V.S., N.G., S.D., D.I.) diinz@psb.vib-ugent.be.
authors.forename: Dirk
authors.identifier: 0000-0002-3217-8407
authors.initials: D
authors.lastname: Inzé
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000254:growth & development* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D049109:Cell Proliferation / Q000187:drug effects; D002736:Chloroplasts / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D058503:Mesophyll Cells / Q000187:drug effects; D009004:Monosaccharide Transport Proteins / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D018515:Plant Leaves / Q000166:cytology / Q000254:growth & development* / Q000378:metabolism; D036226:Seedlings / Q000187:drug effects / Q000254:growth & development; D013395:Sucrose / Q000378:metabolism* / Q000494:pharmacology
chemical_list: D029681:Arabidopsis Proteins; C000592795:GPT2 protein, Arabidopsis; D009004:Monosaccharide Transport Proteins; D013395:Sucrose