Structure of the Mg-Chelatase Cofactor GUN4 Reveals a Novel Hand-Shaped Fold for Porphyrin Binding

Verdecia, Mark A.; Larkin, Robert M.; Ferrer, Jean-Luc; Riek, Roland; Chory, Joanne; Noel, Joseph P.

doi:10.1371/journal.pbio.0030151

Title: Structure of the Mg-Chelatase Cofactor GUN4 Reveals a Novel Hand-Shaped Fold for Porphyrin Binding

Journal Article · 26 April 2005 · PLoS Biology (Online)

DOI: https://doi.org/10.1371/journal.pbio.0030151 · OSTI ID:1627139

Verdecia, Mark A. ^[1]; Larkin, Robert M. ^[1]; Ferrer, Jean-Luc ^[2]; Riek, Roland ^[1]; Chory, Joanne ^[1]; Noel, Joseph P. ^[1]

Salk Institute for Biological Studies, La Jolla, CA (United States)
The Institut de Biologie Structurale, Grenoble (France)

In plants, the accumulation of the chlorophyll precursor Mg-protoporphyrin IX (Mg-Proto) in the plastid regulates the expression of a number of nuclear genes with functions related to photosynthesis. Analysis of the plastid-to-nucleus signaling activity of Mg-Proto in Arabidopsis thaliana led to the discovery of GUN4, a novel porphyrin-binding protein that also dramatically enhances the activity of Mg-chelatase, the enzyme that synthesizes Mg-Proto. GUN4 may also play a role in both photoprotection and the cellular shuttling of tetrapyrroles. Here we report a 1.78-Å resolution crystal structure of Synechocystis GUN4, in which the porphyrin-binding domain adopts a unique three dimensional fold with a ‘‘cupped hand’’ shape. Biophysical and biochemical analyses revealed the specific site of interaction between GUN4 and Mg-Proto and the energetic determinants for the GUN4 • Mg-Proto interaction. Our data support a novel protective function for GUN4 in tetrapyrrole trafficking. The combined structural and energetic analyses presented herein form the physical-chemical basis for understanding GUN4 biological activity, including its role in the stimulation of Mg-chelatase activity, as well as in Mg-Proto retrograde signaling.

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Research Organization:: Salk Institute for Biological Studies, La Jolla, CA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH); National Cancer Institute (NCI); National Science Foundation (NSF)

Grant/Contract Number:: 0236027; CA54418

OSTI ID:: 1627139

Journal Information:: PLoS Biology (Online), Vol. 3, Issue 5; ISSN 1545-7885

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (74)

The importance of porphyrin distortions for the ferrochelatase reaction Sigfridsson, Emma; Ryde, Ulf JBIC Journal of Biological Inorganic Chemistry, Vol. 8, Issue 3 https://doi.org/10.1007/s00775-002-0413-8	journal	February 2003
Regulation of light-harvesting chlorophyll-binding protein mRNA accumulation in Chlamydomonas reinhardi. Possible involvement of chlorophyll synthesis precursors. Johanningmeier, U.; Howell, S. H. Journal of Biological Chemistry, Vol. 259, Issue 21 https://doi.org/10.1016/S0021-9258(18)90727-1	journal	November 1984
Breakdown of thylakoid pigments by soluble proteins of developing chloroplasts Whyte, B. J.; Castelfranco, P. A. Biochemical Journal, Vol. 290, Issue 2 https://doi.org/10.1042/bj2900361	journal	March 1993
Development and validation of a genetic algorithm for flexible docking 1 1Edited by F. E. Cohen Jones, Gareth; Willett, Peter; Glen, Robert C. Journal of Molecular Biology, Vol. 267, Issue 3 https://doi.org/10.1006/jmbi.1996.0897	journal	April 1997
Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch Richly, E.; Dietzmann, A.; Biehl, A. EMBO reports, Vol. 4, Issue 5 https://doi.org/10.1038/sj.embor.embor828	journal	May 2003
GUN4, a Regulator of Chlorophyll Synthesis and Intracellular Signaling Larkin, R. M. Science, Vol. 299, Issue 5608 https://doi.org/10.1126/science.1079978	journal	February 2003
Dissection of Malonyl-Coenzyme A Decarboxylation from Polyketide Formation in the Reaction Mechanism of a Plant Polyketide Synthase ^† Jez, Joseph M.; Ferrer, Jean-Luc; Bowman, Marianne E. Biochemistry, Vol. 39, Issue 5 https://doi.org/10.1021/bi991489f	journal	February 2000
TspO as a Modulator of the Repressor/Antirepressor (PpsR/AppA) Regulatory System in Rhodobacter sphaeroides 2.4.1 Zeng, Xiaohua; Kaplan, Samuel Journal of Bacteriology, Vol. 183, Issue 21 https://doi.org/10.1128/JB.183.21.6355-6364.2001	journal	November 2001
A Novel Mechanism for the Regulation of Photosynthesis Gene Expression by the TspO Outer Membrane Protein of Rhodobacter sphaeroides 2.4.1 Yeliseev, Alexei A.; Kaplan, Samuel Journal of Biological Chemistry, Vol. 274, Issue 30 https://doi.org/10.1074/jbc.274.30.21234	journal	July 1999
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination Brünger, A. T.; Adams, P. D.; Clore, G. M. Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 5 https://doi.org/10.1107/S0907444998003254	journal	September 1998
Pathways of intracellular communication: Tetrapyrroles and plastid-to-nucleus signaling Rodermel, Steve; Park, Sungsoon BioEssays, Vol. 25, Issue 7 https://doi.org/10.1002/bies.10308	journal	June 2003
Travelling of proteins through membranes: translocation into chloroplasts Schleiff, Enrico; Soll, Jürgen Planta, Vol. 211, Issue 4 https://doi.org/10.1007/s004250000357	journal	September 2000
Amitrole treatment of etiolated barley seedlings leads to deregulation of tetrapyrrole synthesis and to reduced expression of Lhc and RbcS genes La Rocca, N.; Rascio, N.; Oster, U. Planta, Vol. 213, Issue 1 https://doi.org/10.1007/s004250000477	journal	May 2001
Structural and mechanistic basis of porphyrin metallation by ferrochelatase Lecerof, D.; Fodje, M.; Hansson, A. Journal of Molecular Biology, Vol. 297, Issue 1 https://doi.org/10.1006/jmbi.2000.3569	journal	March 2000
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1 Ogawa, K. The EMBO Journal, Vol. 20, Issue 11 https://doi.org/10.1093/emboj/20.11.2835	journal	June 2001
Improved methods for building protein models in electron density maps and the location of errors in these models Jones, T. A.; Zou, J. Y.; Cowan, S. W. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 2, p. 110-119 https://doi.org/10.1107/S0108767390010224	journal	March 1991
Interactions between porphyrins and mitochondrial benzodiazepine receptors Kessel, David Cancer Letters, Vol. 39, Issue 2 https://doi.org/10.1016/0304-3835(88)90104-8	journal	March 1988
Solubilization and reconstitution of the mitochondrial benzodiazepine receptor Anholt, Robert R. H.; Aebi, Ueli; Pedersen, Peter L. Biochemistry, Vol. 25, Issue 8 https://doi.org/10.1021/bi00356a041	journal	April 1986
Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC68031 Jensen, Poul E.; Gibson, Lucien C. D.; Hunter, C. Neil Biochemical Journal, Vol. 334, Issue 2 https://doi.org/10.1042/bj3340335	journal	September 1998
Touring protein fold space with Dali/FSSP Holm, L. Nucleic Acids Research, Vol. 26, Issue 1 https://doi.org/10.1093/nar/26.1.316	journal	January 1998
MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures Kraulis, P. J. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S0021889891004399	journal	October 1991
Biosynthesis of chlorophylls from protoporphyrin IX Willows, Robert D. Natural Product Reports, Vol. 20, Issue 3 https://doi.org/10.1039/b110549n	journal	January 2003
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Signal transduction mutants of arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development Susek, Ronald E.; Ausubel, Frederick M.; Chory, Joanne Cell, Vol. 74, Issue 5 https://doi.org/10.1016/0092-8674(93)90459-4	journal	September 1993
Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX Strand, Åsa; Asami, Tadao; Alonso, Jose Nature, Vol. 421, Issue 6918 https://doi.org/10.1038/nature01204	journal	January 2003
The gun4 gene is essential for cyanobacterial porphyrin metabolism Wilde, Annegret; Mikolajczyk, Sandra; Alawady, Ali FEBS Letters, Vol. 571, Issue 1-3 https://doi.org/10.1016/j.febslet.2004.06.063	journal	July 2004
Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus Kropat, Janette; Oster, Ulrike; Rudiger, Wolfhart The Plant Journal, Vol. 24, Issue 4 https://doi.org/10.1046/j.1365-313x.2000.00898.x	journal	November 2000
Mitochondrial Signaling Butow, Ronald A.; Avadhani, Narayan G. Molecular Cell, Vol. 14, Issue 1 https://doi.org/10.1016/S1097-2765(04)00179-0	journal	April 2004
Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.) Cornah, Johanna E.; Roper, Jennifer M.; Singh, Davinder Pal Biochemical Journal, Vol. 362, Issue 2 https://doi.org/10.1042/bj3620423	journal	February 2002
Maximum-likelihood density modification Terwilliger, Thomas C. Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 8 https://doi.org/10.1107/S0907444900005072	journal	August 2000
Measurement of Heme Efflux and Heme Content in Isolated Developing Chloroplasts Thomas, Jim; Weinstein, Jon D. Plant Physiology, Vol. 94, Issue 3 https://doi.org/10.1104/pp.94.3.1414	journal	November 1990
The greening process in cress seedlings. V. Possible interference of chlorophyll precursors, accumulated after thujaplicin treatment, with light-regulated expression of Lhc genes Oster, Ulrike; Brunner, Harald; Rüdiger, Wolfhart Journal of Photochemistry and Photobiology B: Biology, Vol. 36, Issue 3 https://doi.org/10.1016/S1011-1344(96)07388-5	journal	December 1996
TPR proteins: the versatile helix D'Andrea, L. Trends in Biochemical Sciences, Vol. 28, Issue 12 https://doi.org/10.1016/j.tibs.2003.10.007	journal	December 2003
Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator Zhang, L.; Hach, A. Cellular and Molecular Life Sciences (CMLS), Vol. 56, Issue 5-6 https://doi.org/10.1007/s000180050442	journal	November 1999
The peripheral-type benzodiazepine receptor is functionally linked to Leydig cell steroidogenesis. Papadopoulos, V.; Mukhin, A. G.; Costa, E. Journal of Biological Chemistry, Vol. 265, Issue 7 https://doi.org/10.1016/S0021-9258(19)39661-9	journal	March 1990
Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes Kropat, J.; Oster, U.; Rudiger, W. Proceedings of the National Academy of Sciences, Vol. 94, Issue 25 https://doi.org/10.1073/pnas.94.25.14168	journal	December 1997
Pathways of plastid-to-nucleus signaling Rodermel, Steve Trends in Plant Science, Vol. 6, Issue 10 https://doi.org/10.1016/S1360-1385(01)02085-4	journal	October 2001
Inactivation of Mg Chelatase during Transition from Anaerobic to Aerobic Growth in Rhodobacter capsulatus Willows, Robert D.; Lake, Vanessa; Roberts, Thomas Hugh Journal of Bacteriology, Vol. 185, Issue 11 https://doi.org/10.1128/JB.185.11.3249-3258.2003	journal	June 2003
TspO of Rhodobacter sphaeroides: A STRUCTURAL AND FUNCTIONAL MODEL FOR THE MAMMALIAN PERIPHERAL BENZODIAZEPINE RECEPTOR Yeliseev, Alexei A.; Kaplan, Samuel Journal of Biological Chemistry, Vol. 275, Issue 8 https://doi.org/10.1074/jbc.275.8.5657	journal	February 2000
Phosphoserine/threonine-binding domains Yaffe, Michael B.; Elia, Andrew E. H. Current Opinion in Cell Biology, Vol. 13, Issue 2 https://doi.org/10.1016/S0955-0674(00)00189-7	journal	April 2001
Contact-shifted resonances in the 1H NMR spectra of cytochrome b5 Resonance identification and spin density distribution in the heme group Keller, Regula; Groudinsky, Olga; Wüthrich, Kurt Biochimica et Biophysica Acta (BBA) - Protein Structure, Vol. 427, Issue 2 https://doi.org/10.1016/0005-2795(76)90192-6	journal	April 1976
Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC6803. II. Sequence Determination of the Entire Genome and Assignment of Potential Protein-coding Regions Kaneko, T.; Sato, S.; Kotani, H. DNA Research, Vol. 3, Issue 3 https://doi.org/10.1093/dnares/3.3.109	journal	January 1996
Protoporphyrin IX binding and transport by recombinant mouse PBR Wendler, Gregor; Lindemann, Peter; Lacapère, Jean-Jacques Biochemical and Biophysical Research Communications, Vol. 311, Issue 4 https://doi.org/10.1016/j.bbrc.2003.10.070	journal	November 2003
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Automated MAD and MIR structure solution Terwilliger, Thomas C.; Berendzen, Joel Acta Crystallographica Section D Biological Crystallography, Vol. 55, Issue 4 https://doi.org/10.1107/S0907444999000839	journal	April 1999
Characterization of the Binding of Deuteroporphyrin IX to the Magnesium Chelatase H Subunit and Spectroscopic Properties of the Complex Karger, Guy A.; Reid, James D.; Hunter, C. Neil Biochemistry, Vol. 40, Issue 31 https://doi.org/10.1021/bi010562a	journal	July 2001
Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons Nicholls, Anthony; Sharp, Kim A.; Honig, Barry Proteins: Structure, Function, and Genetics, Vol. 11, Issue 4 https://doi.org/10.1002/prot.340110407	journal	December 1991
Pathways of intracellular communication: Tetrapyrroles and plastid-to-nucleus signaling Rodermel, Steve; Park, Sungsoon BioEssays, Vol. 25, Issue 7 https://doi.org/10.1002/bies.10308	journal	June 2003
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons Nicholls, Anthony; Sharp, Kim A.; Honig, Barry Proteins: Structure, Function, and Genetics, Vol. 11, Issue 4 https://doi.org/10.1002/prot.340110407	journal	December 1991
Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator Zhang, L.; Hach, A. Cellular and Molecular Life Sciences (CMLS), Vol. 56, Issue 5-6 https://doi.org/10.1007/s000180050442	journal	November 1999
Travelling of proteins through membranes: translocation into chloroplasts Schleiff, Enrico; Soll, Jürgen Planta, Vol. 211, Issue 4 https://doi.org/10.1007/s004250000357	journal	September 2000
The importance of porphyrin distortions for the ferrochelatase reaction Sigfridsson, Emma; Ryde, Ulf JBIC Journal of Biological Inorganic Chemistry, Vol. 8, Issue 3 https://doi.org/10.1007/s00775-002-0413-8	journal	February 2003
Signal transduction mutants of arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development Susek, Ronald E.; Ausubel, Frederick M.; Chory, Joanne Cell, Vol. 74, Issue 5 https://doi.org/10.1016/0092-8674(93)90459-4	journal	September 1993
Interactions between porphyrins and mitochondrial benzodiazepine receptors Kessel, David Cancer Letters, Vol. 39, Issue 2 https://doi.org/10.1016/0304-3835(88)90104-8	journal	March 1988
Protoporphyrin IX binding and transport by recombinant mouse PBR Wendler, Gregor; Lindemann, Peter; Lacapère, Jean-Jacques Biochemical and Biophysical Research Communications, Vol. 311, Issue 4 https://doi.org/10.1016/j.bbrc.2003.10.070	journal	November 2003
Regulation of protein synthesis by heme-regulated eIF-2α kinase Chen, Jane-Jane; London, Irving M. Trends in Biochemical Sciences, Vol. 20, Issue 3 https://doi.org/10.1016/s0968-0004(00)88975-6	journal	March 1995
Interaction between the Bacterial Iron Response Regulator and Ferrochelatase Mediates Genetic Control of Heme Biosynthesis Qi, Zhenhao; O'Brian, Mark R. Molecular Cell, Vol. 9, Issue 1 https://doi.org/10.1016/s1097-2765(01)00431-2	journal	January 2002
Dissection of Malonyl-Coenzyme A Decarboxylation from Polyketide Formation in the Reaction Mechanism of a Plant Polyketide Synthase ^† Jez, Joseph M.; Ferrer, Jean-Luc; Bowman, Marianne E. Biochemistry, Vol. 39, Issue 5 https://doi.org/10.1021/bi991489f	journal	February 2000
Covariations in the nuclear chloroplast transcriptome reveal a regulatory master-switch Richly, E.; Dietzmann, A.; Biehl, A. EMBO reports, Vol. 4, Issue 5 https://doi.org/10.1038/sj.embor.embor828	journal	May 2003
Biosynthesis of chlorophylls from protoporphyrin IX Willows, Robert D. Natural Product Reports, Vol. 20, Issue 3 https://doi.org/10.1039/b110549n	journal	January 2003
Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L.) E. Cornah, Johanna; M. Roper, Jennifer; Pal SINGH, Davinder Biochemical Journal, Vol. 362, Issue 2 https://doi.org/10.1042/0264-6021:3620423	journal	March 2002
Breakdown of thylakoid pigments by soluble proteins of developing chloroplasts Whyte, B. J.; Castelfranco, P. A. Biochemical Journal, Vol. 290, Issue 2 https://doi.org/10.1042/bj2900361	journal	March 1993
Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC68031 Jensen, Poul E.; Gibson, Lucien C. D.; Hunter, C. Neil Biochemical Journal, Vol. 334, Issue 2 https://doi.org/10.1042/bj3340335	journal	September 1998
Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus Kropat, Janette; Oster, Ulrike; Rudiger, Wolfhart The Plant Journal, Vol. 24, Issue 4 https://doi.org/10.1046/j.1365-313x.2000.00898.x	journal	November 2000
Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes Kropat, J.; Oster, U.; Rudiger, W. Proceedings of the National Academy of Sciences, Vol. 94, Issue 25 https://doi.org/10.1073/pnas.94.25.14168	journal	December 1997
Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction Mochizuki, N.; Brusslan, J. A.; Larkin, R. Proceedings of the National Academy of Sciences, Vol. 98, Issue 4 https://doi.org/10.1073/pnas.98.4.2053	journal	February 2001
A Soluble Form of the First Extracellular Domain of Mouse Type 2β Corticotropin-releasing Factor Receptor Reveals Differential Ligand Specificity Perrin, Marilyn H.; DiGruccio, Michael R.; Koerber, Steven C. Journal of Biological Chemistry, Vol. 278, Issue 18 https://doi.org/10.1074/jbc.m210476200	journal	May 2003
Signaling the Unfolded Protein Response from the Endoplasmic Reticulum Zhang, Kezhong; Kaufman, Randal J. Journal of Biological Chemistry, Vol. 279, Issue 25 https://doi.org/10.1074/jbc.r400008200	journal	June 2004
Sequence Analysis of the Genome of the Unicellular Cyanobacterium Synechocystis sp. Strain PCC6803. II. Sequence Determination of the Entire Genome and Assignment of Potential Protein-coding Regions Kaneko, T.; Sato, S.; Kotani, H. DNA Research, Vol. 3, Issue 3 https://doi.org/10.1093/dnares/3.3.109	journal	January 1996
Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1 Ogawa, K. The EMBO Journal, Vol. 20, Issue 11 https://doi.org/10.1093/emboj/20.11.2835	journal	June 2001
Touring protein fold space with Dali/FSSP Holm, L. Nucleic Acids Research, Vol. 26, Issue 1 https://doi.org/10.1093/nar/26.1.316	journal	January 1998
GUN4, a Regulator of Chlorophyll Synthesis and Intracellular Signaling Larkin, R. M. Science, Vol. 299, Issue 5608 https://doi.org/10.1126/science.1079978	journal	February 2003

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59 BASIC BIOLOGICAL SCIENCES
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Title: Structure of the Mg-Chelatase Cofactor GUN4 Reveals a Novel Hand-Shaped Fold for Porphyrin Binding

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