title: Chloroplast FBPase and SBPase are thioredoxin-linked enzymes with similar architecture but different evolutionary histories.
abstract: The Calvin-Benson cycle of carbon dioxide fixation in chloroplasts is controlled by light-dependent redox reactions that target specific enzymes. Of the regulatory members of the cycle, our knowledge of sedoheptulose-1,7-bisphosphatase (SBPase) is particularly scanty, despite growing evidence for its importance and link to plant productivity. To help fill this gap, we have purified, crystallized, and characterized the recombinant form of the enzyme together with the better studied fructose-1,6-bisphosphatase (FBPase), in both cases from the moss Physcomitrella patens (Pp). Overall, the moss enzymes resembled their counterparts from seed plants, including oligomeric organization-PpSBPase is a dimer, and PpFBPase is a tetramer. The two phosphatases showed striking structural homology to each other, differing primarily in their solvent-exposed surface areas in a manner accounting for their specificity for seven-carbon (sedoheptulose) and six-carbon (fructose) sugar bisphosphate substrates. The two enzymes had a similar redox potential for their regulatory redox-active disulfides (-310 mV for PpSBPase vs. -290 mV for PpFBPase), requirement for Mg(2+) and thioredoxin (TRX) specificity (TRX f > TRX m). Previously known to differ in the position and sequence of their regulatory cysteines, the enzymes unexpectedly showed unique evolutionary histories. The FBPase gene originated in bacteria in conjunction with the endosymbiotic event giving rise to mitochondria, whereas SBPase arose from an archaeal gene resident in the eukaryotic host. These findings raise the question of how enzymes with such different evolutionary origins achieved structural similarity and adapted to control by the same light-dependent photosynthetic mechanism-namely ferredoxin, ferredoxin-thioredoxin reductase, and thioredoxin.
authors.affiliation: Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France; Spemann Graduate School of Biology and Medicine, University of Freiburg, 79104 Freiburg, Germany;
authors.forename: Desirée D
authors.initials: DD
authors.lastname: Gütle
authors.affiliation: Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France;
authors.forename: Thomas
authors.initials: T
authors.lastname: Roret
authors.affiliation: Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany;
authors.forename: Stefanie J
authors.initials: SJ
authors.lastname: Müller
authors.affiliation: Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France;
authors.forename: Jérémy
authors.initials: J
authors.lastname: Couturier
authors.affiliation: Sorbonne Universités, Université Pierre et Marie Curie (UPMC) Université Paris 6, CNRS UMR 8226, Laboratoire de Biologie Moléculaire et Cellulaire des Eucaryotes, Institut de Biologie Physico-Chimique, 75005 Paris, France;
authors.forename: Stéphane D
authors.initials: SD
authors.lastname: Lemaire
authors.affiliation: Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France;
authors.forename: Arnaud
authors.initials: A
authors.lastname: Hecker
authors.affiliation: Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France;
authors.forename: Tiphaine
authors.initials: T
authors.lastname: Dhalleine
authors.affiliation: Department of Plant & Microbial Biology, University of California, Berkeley, CA 94720-3102; j2p@univ-lorraine.fr view@berkeley.edu.
authors.forename: Bob B
authors.initials: BB
authors.lastname: Buchanan
authors.affiliation: Plant Biotechnology, Faculty of Biology, University of Freiburg, 79104 Freiburg, Germany; Spemann Graduate School of Biology and Medicine, University of Freiburg, 79104 Freiburg, Germany; Centre for Biological Signalling Studies (BIOSS), 79104 Freiburg, Germany; Freiburg Institute for Advanced Studies (FRIAS), 79104 Freiburg, Germany;
authors.forename: Ralf
authors.initials: R
authors.lastname: Reski
authors.affiliation: Spemann Graduate School of Biology and Medicine, University of Freiburg, 79104 Freiburg, Germany; Centre for Biological Signalling Studies (BIOSS), 79104 Freiburg, Germany; Freiburg Institute for Advanced Studies (FRIAS), 79104 Freiburg, Germany; Institute for Biochemistry, University of Freiburg, 79104 Freiburg, Germany.
authors.forename: Oliver
authors.initials: O
authors.lastname: Einsle
authors.affiliation: Université de Lorraine, UMR 1136 Interactions Arbres Microorganismes, F-54500 Vandœuvre-les-Nancy, France; Institut national de la recherche agronomique (INRA), UMR 1136 Interactions Arbres Microorganismes, F-54280 Champenoux, France; j2p@univ-lorraine.fr view@berkeley.edu.
authors.forename: Jean-Pierre
authors.identifier: 0000-0003-4975-8587
authors.initials: JP
authors.lastname: Jacquot
mesh_terms: D019068:Bryopsida / Q000201:enzymology / Q000235:genetics; D060365:Chloroplast Proteins / Q000235:genetics / Q000378:metabolism; D019143:Evolution, Molecular; D006597:Fructose-Bisphosphatase / Q000235:genetics / Q000378:metabolism; D010744:Phosphoric Monoester Hydrolases / Q000235:genetics / Q000378:metabolism; D013879:Thioredoxins / Q000235:genetics / Q000378:metabolism
chemical_list: D060365:Chloroplast Proteins; D013879:Thioredoxins; D006597:Fructose-Bisphosphatase; D010744:Phosphoric Monoester Hydrolases; C022627:sedoheptulose-bisphosphatase
keywords: Calvin–Benson cycle; fructose-1,6-bisphosphatase; redox regulation; sedoheptulose-1,7-bisphosphatase; thiol–disulfide exchange