Thioredoxin f1 and NADPH-Dependent Thioredoxin Reductase C Have Overlapping Functions in Regulating Photosynthetic Metabolism and Plant Growth in Response to Varying Light Conditions.
Two different thiol redox systems exist in plant chloroplasts, the ferredoxin-thioredoxin (Trx) system, which depends on ferredoxin reduced by the photosynthetic electron transport chain and, thus, on light, and the NADPH-dependent Trx reductase C (NTRC) system, which relies on NADPH and thus may be linked to sugar metabolism in the dark. Previous studies suggested, therefore, that the two different systems may have different functions in plants. We now report that there is a previously unrecognized functional redundancy of Trx f1 and NTRC in regulating photosynthetic metabolism and growth. In Arabidopsis (Arabidopsis thaliana) mutants, combined, but not single, deficiencies of Trx f1 and NTRC led to severe growth inhibition and perturbed light acclimation, accompanied by strong impairments of Calvin-Benson cycle activity and starch accumulation. Light activation of key enzymes of these pathways, fructose-1,6-bisphosphatase and ADP-glucose pyrophosphorylase, was almost completely abolished. The subsequent increase in NADPH-NADP(+) and ATP-ADP ratios led to increased nitrogen assimilation, NADP-malate dehydrogenase activation, and light vulnerability of photosystem I core proteins. In an additional approach, reporter studies show that Trx f1 and NTRC proteins are both colocalized in the same chloroplast substructure. Results provide genetic evidence that light- and NADPH-dependent thiol redox systems interact at the level of Trx f1 and NTRC to coordinately participate in the regulation of the Calvin-Benson cycle, starch metabolism, and growth in response to varying light conditions.
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Ina
http://orcid.org/0000-0002-8993-8745
I
Thormählen
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Tobias
http://orcid.org/0000-0002-1020-7107
T
Meitzel
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Julia
http://orcid.org/0000-0003-2070-0330
J
Groysman
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Alexandra Bianca
http://orcid.org/0000-0002-6070-8751
AB
Öchsner
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Edda
E
von Roepenack-Lahaye
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Belén
B
Naranjo
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.).
Francisco J
http://orcid.org/0000-0002-3936-5491
FJ
Cejudo
Department Biologie I, Ludwig-Maximilians-Universität München, 82152 Martinsried, Germany (I.T., J.G., A.B.Ö., E.v.R.-L., P.G.);Leibniz-Institut für Pflanzengenetik und Kulturpflanzenforschung, 06466 Gatersleben, Germany (T.M.); andInstituto de Bioquímica Vegetal y Fotosíntesis, University of Seville and Consejo Superior de Investigaciones Científicas, 41092 Seville, Spain (B.N., F.J.C.) geigenberger@bio.lmu.de.
Peter
http://orcid.org/0000-0001-9512-349X
P
Geigenberger
D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000502:physiology / Q000528:radiation effects; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002736:Chloroplasts / Q000378:metabolism; D051599:Glucose-1-Phosphate Adenylyltransferase / Q000235:genetics / Q000378:metabolism; D050538:Malate Dehydrogenase (NADP+) / Q000235:genetics / Q000378:metabolism; D055442:Metabolome; D010084:Oxidation-Reduction; D010641:Phenotype; D010788:Photosynthesis / Q000528:radiation effects; D045331:Photosystem I Protein Complex / Q000378:metabolism; D018515:Plant Leaves / Q000201:enzymology / Q000235:genetics / Q000502:physiology / Q000528:radiation effects; D018526:Plant Transpiration / Q000528:radiation effects; D013213:Starch / Q000378:metabolism; D013880:Thioredoxin-Disulfide Reductase / Q000235:genetics / Q000378:metabolism*; D013879:Thioredoxins / Q000378:metabolism*
D029681:Arabidopsis Proteins; D045331:Photosystem I Protein Complex; D013879:Thioredoxins; D013213:Starch; D050538:Malate Dehydrogenase (NADP+); D013880:Thioredoxin-Disulfide Reductase; D051599:Glucose-1-Phosphate Adenylyltransferase