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The Maize Oil Yellow1 (Oy1) Gene Encodes the I Subunit of Magnesium Chelatase

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Abstract

Semi-dominant Oil yellow1 (Oy1) mutants of maize (Zea mays) are deficient in the conversion of protoporphyrin IX to magnesium protoporphyrin IX, the first committed step of chlorophyll biosynthesis. Using a candidate gene approach, a cDNA clone was isolated that was predicted to encode the I subunit of magnesium chelatase (ZmCHLI) and mapped to the same genetic interval as Oy1. Allelic variation was identified at ZmCHLI between wild-type plants and plants carrying semi-dominant alleles of Oy1. These differences revealed putative amino acid substitutions that could account for the alterations in protein function. Candidate lesions were tested by introduction of homologous changes into the Synechocystis magnesium chelatase I gene (SschlI) and characterization of the activity of mutant protein variants in an in vitro enzyme activity assay. The results of these analyses suggest that SsChlI protein variants containing the substitutions identified in the dominant Oy1 maize alleles lack activity necessary for magnesium chelation and confer a semi-dominant phenotype via competitive inhibition of wild-type SsChlI.

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Abbreviations

AAA:

ATPases associated with various cellular activities

Fe chelatase:

ferrochelatase

Mg chelatase:

magnesium chelatase

Mg proto IX:

Mg protoporphyrin IX

proto IX:

protoporphyrin IX

References

  • M. Bochtler C. Hartmann H.K. Song G.P. Bourenkov H.D. Bartunik R. Huber (2000) ArticleTitleThe structures of HsIU and the ATP-dependent protease HsIU–HsIV Nature 403 800–805 Occurrence Handle10.1038/35001629 Occurrence Handle1:CAS:528:DC%2BD3cXhsVWiu7s%3D Occurrence Handle10693812

    Article  CAS  PubMed  Google Scholar 

  • J.E. Cornah M.J. Terry A.G. Smith (2003) ArticleTitleGreen or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci. 8 224–230 Occurrence Handle10.1016/S1360-1385(03)00064-5 Occurrence Handle1:CAS:528:DC%2BD3sXjvFWlsLo%3D Occurrence Handle12758040

    Article  CAS  PubMed  Google Scholar 

  • M.J. Davey D. Jeruzalmi J. Kuriyan M. O’Donnell (2002) ArticleTitleMotors and switches: AAA+ machines within the replisome Nat. Rev. Mol. Cell. Biol. 3 826–835 Occurrence Handle10.1038/nrm949 Occurrence Handle1:CAS:528:DC%2BD38Xotlerur4%3D Occurrence Handle12415300

    Article  CAS  PubMed  Google Scholar 

  • P.A. Davison H.L. Schubert J.D. Reid C. Lorg A. Heroux C.P. Hill C.N. Hunter (2005) ArticleTitleStructural and biochemical characterization of GUN4 suggests a mechanism for its role in chlorophyll biosynthesis Biochemistry 44 7603–7612 Occurrence Handle10.1021/bi050240x Occurrence Handle1:CAS:528:DC%2BD2MXjslKlsrY%3D Occurrence Handle15909975

    Article  CAS  PubMed  Google Scholar 

  • H.K. Dooner (2002) ArticleTitleExtensive interallelic polymorphisms drive meiotic recombination into a crossover pathway Plant Cell 14 1173–1183 Occurrence Handle10.1105/tpc.001271 Occurrence Handle1:CAS:528:DC%2BD38XksVGqt74%3D Occurrence Handle12034905

    Article  CAS  PubMed  Google Scholar 

  • O. Emanuelson H. Nielsen S. Brunak G. Heijne Particlevon (2000) ArticleTitlePredicting subcellular localization of protiens based on their N-terminal amino acid sequence J. Mol. Biol. 300 1005–1016

    Google Scholar 

  • M.N. Fodje A. Hansson M. Hansson J.G. Olsen S. Gough R.D. Willows S. Al-Karadaghi (2001) ArticleTitleInterplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase J. Mol. Biol. 311 111–122 Occurrence Handle10.1006/jmbi.2001.4834 Occurrence Handle1:CAS:528:DC%2BD3MXltl2qu7w%3D Occurrence Handle11469861

    Article  CAS  PubMed  Google Scholar 

  • L.C. Gibson P.E. Jensen C.N. Hunter (1999) ArticleTitleMagnesium chelatase from Rhodobacter sphaeroides: initial characterization of the enzyme using purified subunits and evidence for a BchI-BchD complex Biochem. J. 337 IssueID2 243–251 Occurrence Handle10.1042/0264-6021:3370243 Occurrence Handle1:CAS:528:DyaK1MXhtVemurY%3D Occurrence Handle9882621

    Article  CAS  PubMed  Google Scholar 

  • L.C. Gibson J.L. Marrison R.M. Leech P.E. Jensen D.C. Bassham M. Gibson C.N. Hunter (1996) ArticleTitleA putative Mg chelatase subunit from Arabidopsis thaliana cv C24. Sequence and transcript analysis of the gene, import of the protein into chloroplasts, and in situ localization of the transcript and protein Plant Physiol. 111 61–71 Occurrence Handle10.1104/pp.111.1.61 Occurrence Handle1:CAS:528:DyaK28XivFektLs%3D Occurrence Handle8685276

    Article  CAS  PubMed  Google Scholar 

  • L.C. Gibson R.D. Willows C.G. Kannangara D. Wettstein Particlevon C.N. Hunter (1995) ArticleTitleMagnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli Proc. Natl. Acad. Sci. USA 92 1941–1944 Occurrence Handle1:CAS:528:DyaK2MXksVCqs7o%3D Occurrence Handle7892204

    CAS  PubMed  Google Scholar 

  • Grimm B. 2003. Regulatory mechanisms of eukaryotic tetrapyrrole biosynthesis. In: K.M. Kadish, Smith K.M. Smith and R. Guilard (Eds.), The Porphyrin Handbook, New York pp. 1–32.

  • A. Hansson C.G. Kannangara D. Wettstein Particlevon M. Hansson (1999) ArticleTitleMolecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase Proc. Natl. Acad. Sci. USA 96 1744–1749 Occurrence Handle1:CAS:528:DyaK1MXhsFSqtr4%3D Occurrence Handle9990095

    CAS  PubMed  Google Scholar 

  • A. Hansson R.D. Willows T.H. Roberts M. Hansson (2002) ArticleTitleThree semidominant barley mutants with single amino acid substitutions in the smallest magnesium chelatase subunit form defective AAA+ hexamers Proc. Natl. Acad. Sci. USA 99 13944–13949 Occurrence Handle1:CAS:528:DC%2BD38XotVKmu7w%3D Occurrence Handle12357035

    CAS  PubMed  Google Scholar 

  • A. Hudson R. Carpenter S. Doyle E.S. Coen (1993) ArticleTitleOLIVE: a key gene required for chlorophyll biosynthesis in Antirrhinum majus Embo J. 12 3711–3719 Occurrence Handle1:CAS:528:DyaK3sXmsVGlsr8%3D Occurrence Handle8404842

    CAS  PubMed  Google Scholar 

  • L.M. Iyer D.D. Leipe E.V. Koonin L. Aravind (2004) ArticleTitleEvolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 11–31 Occurrence Handle10.1016/j.jsb.2003.10.010 Occurrence Handle1:CAS:528:DC%2BD2cXisVSmtro%3D Occurrence Handle15037234

    Article  CAS  PubMed  Google Scholar 

  • P.E. Jensen L.C. Gibson K.W. Henningsen C.N. Hunter (1996) ArticleTitleExpression of the chlI, chlD, and chlH genes from the Cyanobacterium Synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity J. Biol. Chem. 271 16662–16667 Occurrence Handle1:CAS:528:DyaK28Xkt1Cjsrc%3D Occurrence Handle8663186

    CAS  PubMed  Google Scholar 

  • P.E. Jensen L.C. Gibson C.N. Hunter (1998) ArticleTitleDeterminants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC6803 Biochem. J. 334 IssueID2 335–344 Occurrence Handle1:CAS:528:DyaK1cXmtFOlsL0%3D Occurrence Handle9716491

    CAS  PubMed  Google Scholar 

  • P.E. Jensen L.C. Gibson C.N. Hunter (1999) ArticleTitleATPase activity associated with the magnesium-protoporphyrin IX chelatase enzyme of Synechocystis PCC6803: evidence for ATP hydrolysis during Mg2+ insertion, and the MgATP-dependent interaction of the ChlI and ChlD subunits Biochem. J. 339 IssueID1 127–134 Occurrence Handle10.1042/0264-6021:3390127 Occurrence Handle1:CAS:528:DyaK1MXisFWmurg%3D Occurrence Handle10085236

    Article  CAS  PubMed  Google Scholar 

  • P.E. Jensen R.D. Willows B.L. Petersen U.C. Vothknecht B.M. Stummann C.G. Kannangara D. Wettstein Particlevon K.W. Henningsen (1996) ArticleTitleStructural genes for Mg-chelatase subunits in barley: Xantha-f, -g and -h Mol. Gen. Genet. 250 383–394 Occurrence Handle1:CAS:528:DyaK28XitVKrsrw%3D Occurrence Handle8602155

    CAS  PubMed  Google Scholar 

  • C.G. Kannangara U.C. Vothknecht M. Hansson D. Wettstein Particlevon (1997) ArticleTitleMagnesium chelatase: association with ribosomes and mutant complementation studies identify barley subunit XANTHA-G as a functional counterpart of Rhodobacter subunit BchD Mol. Gen. Genet. 254 85–92 Occurrence Handle1:CAS:528:DyaK2sXjsFGjsb0%3D Occurrence Handle9108294

    CAS  PubMed  Google Scholar 

  • G.A. Karger J.D. Reid C.N. Hunter (2001) ArticleTitleCharacterization of the binding of deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex Biochemistry 40 9291–9299 Occurrence Handle10.1021/bi010562a Occurrence Handle1:CAS:528:DC%2BD3MXltVyjuro%3D Occurrence Handle11478896

    Article  CAS  PubMed  Google Scholar 

  • K.I. Kim G.W. Cheong S.C. Park J.S. Ha K.M. Woo S.J. Choi C.H. Chung (2000) ArticleTitleHeptameric ring structure of the heat-shock protein ClpB, a protein-activated ATPase in Escherichia coli J. Mol. Biol. 303 655–666 Occurrence Handle1:CAS:528:DC%2BD3cXnslCqsbo%3D Occurrence Handle11061966

    CAS  PubMed  Google Scholar 

  • S. Kjemtrup K.S. Sampson C.G. Peele L.V. Nguyen M.A. Conkling W.F. Thompson D. Robertson (1998) ArticleTitleGene silencing from plant DNA carried by a geminivirus Plant J. 14 91–100 Occurrence Handle10.1046/j.1365-313X.1998.00101.x Occurrence Handle1:CAS:528:DyaK1cXjtV2isL8%3D Occurrence Handle15494056

    Article  CAS  PubMed  Google Scholar 

  • C. Koncz R. Mayerhofer Z. Koncz-Kalman C. Nawrath B. Reiss G.P. Redei J. Schell (1990) ArticleTitleIsolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana Embo J. 9 1337–1346 Occurrence Handle1:CAS:528:DyaK3cXls1KnsL4%3D Occurrence Handle2158442

    CAS  PubMed  Google Scholar 

  • R.M. Larkin J.M. Alonso J.R. Ecker J. Chory (2003) ArticleTitleGUN4, a regulator of chlorophyll synthesis and intracellular signaling Science 299 902–906 Occurrence Handle10.1126/science.1079978 Occurrence Handle1:CAS:528:DC%2BD3sXpt1SgsQ%3D%3D Occurrence Handle12574634

    Article  CAS  PubMed  Google Scholar 

  • D. Lecerof M.N. Fodje R. Alvarez Leon U. Olsson A. Hansson E. Sigfridsson U. Ryde M. Hansson S Al-Karadaghi (2003) ArticleTitleMetal binding to Bacillus subtilis ferrochelatase and interaction between metal sites J. Biol. Inorg. Chem. 8 452–458 Occurrence Handle1:CAS:528:DC%2BD3sXjvFCjsbk%3D Occurrence Handle12761666

    CAS  PubMed  Google Scholar 

  • E.W. Lindstrom (1935) ArticleTitleSome new mutants in maize Iowa State Coll. J. Sci. 9 451–459

    Google Scholar 

  • P.N. Mascia (1978) ArticleTitleGenetic studies of luteus mutants MNL 52 56–58

    Google Scholar 

  • P.N. Mascia D.S. Robertson (1980) ArticleTitleGenetic studies of the chlorophyll biosynthetic mutants of maize J. Hered. 71 19–24 Occurrence Handle1:CAS:528:DyaL3cXksVWksbs%3D

    CAS  Google Scholar 

  • E.C. Matz F. Burr B. Burr (1992) ArticleTitleRFLP mapping of mutants MNL 66 107

    Google Scholar 

  • N. Mochizuki J.A. Brusslan R. Larkin A. Nagatani J. Chory (2001) ArticleTitleArabidopsis genomes uncoupled 5 (gun5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction Proc. Natl. Acad. Sci. USA 98 2053–2058 Occurrence Handle1:CAS:528:DC%2BD3MXhsVWit7c%3D Occurrence Handle11172074

    CAS  PubMed  Google Scholar 

  • M.G. Neuffer D.J. England (1995) ArticleTitleInduced mutations with confirmed locations MNL 69 43–46

    Google Scholar 

  • Nguyen, L.V. 1995. Transposon Tagging and Isolation of the SULFUR Gene in Tobacco (Nicotiana tabacum). North Carolina State University.

  • T. Ogura A.J. Wilkinson (2001) ArticleTitleAAA+ superfamily ATPases: common structure-diverse function Genes Cells 6 575–597 Occurrence Handle10.1046/j.1365-2443.2001.00447.x Occurrence Handle1:CAS:528:DC%2BD3MXlvFKktLs%3D Occurrence Handle11473577

    Article  CAS  PubMed  Google Scholar 

  • L.E. Palmer P.D. Rabinowicz A.L. O’Shaughnessy V.S. Balija L.U. Nascimento S. Dike M. la Bastide Particlede R.A. Martienssen W.R. McCombie (2003) ArticleTitleMaize genome sequencing by methylation filtration Science 302 2115–2117 Occurrence Handle10.1126/science.1091265 Occurrence Handle14684820

    Article  PubMed  Google Scholar 

  • J.D. Reid C.N. Hunter (2004) ArticleTitleMagnesium-dependent ATPase activity and cooperativity of magnesium chelatase from Synechocystis sp. PCC6803 J. Biol. Chem. 279 26893–26899 Occurrence Handle1:CAS:528:DC%2BD2cXkvFGgu7g%3D Occurrence Handle15051720

    CAS  PubMed  Google Scholar 

  • J.D. Reid C.A. Siebert P.A. Bullough C.N. Hunter (2003) ArticleTitleThe ATPase activity of the ChlI subunit of magnesium chelatase and formation of a heptameric AAA+ ring Biochemistry 42 6912–6920 Occurrence Handle1:CAS:528:DC%2BD3sXjs12qsb4%3D Occurrence Handle12779346

    CAS  PubMed  Google Scholar 

  • R.J. Sawers P.J. Linley J.F. Gutierrez-Marcos T. Delli-Bovi P.R. Farmer T. Kohchi M.J. Terry T.P. Brutnell (2004) ArticleTitleThe Elm1 (ZmHy2) gene of maize encodes a phytochromobilin synthase Plant Physiol. 136 2771–2781 Occurrence Handle10.1104/pp.104.046417 Occurrence Handle1:CAS:528:DC%2BD2cXnvFOqsr0%3D Occurrence Handle15347785

    Article  CAS  PubMed  Google Scholar 

  • D. St Johnston (2002) ArticleTitleThe art and design of genetic screens: Drosophila melanogaster Nat. Rev. Genet. 3 176–188 Occurrence Handle10.1038/nrg751 Occurrence Handle1:CAS:528:DC%2BD38Xit1Cks7w%3D Occurrence Handle11972155

    Article  CAS  PubMed  Google Scholar 

  • A. Strand (2004) ArticleTitlePlastid-to-nucleus signalling Curr. Opin. Plant Biol. 7 621–625 Occurrence Handle10.1016/j.pbi.2004.09.004 Occurrence Handle1:CAS:528:DC%2BD2cXos1ChsLs%3D Occurrence Handle15491909

    Article  CAS  PubMed  Google Scholar 

  • A. Strand T. Asami J. Alonso J.R. Ecker J. Chory (2003) ArticleTitleChloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX Nature 421 79–83 Occurrence Handle10.1038/nature01204 Occurrence Handle1:CAS:528:DC%2BD3sXos10%3D Occurrence Handle12511958

    Article  CAS  PubMed  Google Scholar 

  • M.I. Tenaillon M.C. Sawkins L.K. Anderson S.M. Stack J. Doebley B.S. Gaut (2002) ArticleTitlePatterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.) Genetics 162 1401–1413 Occurrence Handle1:CAS:528:DC%2BD38XpslCisrs%3D Occurrence Handle12454083

    CAS  PubMed  Google Scholar 

  • J.M. Thornsberry M.M. Goodman J. Doebley S. Kresovich D. Nielsen E.S. Buckler (2001) ArticleTitleDwarf8 polymorphisms associate with variation in flowering time Nat. Genet. 28 286–289 Occurrence Handle10.1038/90135 Occurrence Handle1:CAS:528:DC%2BD3MXltFSmurc%3D Occurrence Handle11431702

    Article  CAS  PubMed  Google Scholar 

  • R.D. Vale (2000) ArticleTitleAAA proteins. Lords of the ring J. Cell. Biol. 150 F13–F19 Occurrence Handle10.1083/jcb.150.1.F13 Occurrence Handle1:CAS:528:DC%2BD3cXltVGhsb8%3D Occurrence Handle10893253

    Article  CAS  PubMed  Google Scholar 

  • C.J. Walker R.D. Willows (1997) ArticleTitleMechanism and regulation of Mg-chelatase Biochem J. 327 IssueID2 321–333 Occurrence Handle1:CAS:528:DyaK2sXntVyls78%3D Occurrence Handle9359397

    CAS  PubMed  Google Scholar 

  • C.A. Whitelaw W.B. Barbazuk G. Pertea A.P. Chan F. Cheung Y. Lee L. Zheng S. Heeringen Particlevan S. Karamycheva J.L. Bennetzen P. SanMiguel N. Lakey J. Bedell Y. Yuan M.A. Budiman A. Resnick S. Aken ParticleVan T. Utterback S. Riedmuller M. Williams T. Feldblyum K. Schubert R. Beachy C.M. Fraser J. Quackenbush (2003) ArticleTitleEnrichment of gene-coding sequences in maize by genome filtration Science 302 2118–2120 Occurrence Handle10.1126/science.1090047 Occurrence Handle14684821

    Article  PubMed  Google Scholar 

  • S.R. Whitt L.M. Wilson M.I. Tenaillon B.S. Gaut E.S. Buckler (2002) ArticleTitleGenetic diversity and selection in the maize starch pathway Proc. Natl. Acad. Sci. USA 99 12959–12962 Occurrence Handle10.1073/pnas.202476999 Occurrence Handle1:CAS:528:DC%2BD38XnvFGht7Y%3D Occurrence Handle12244216

    Article  CAS  PubMed  Google Scholar 

  • A. Wilde S. Mikolajczyka A. Alawady H. Lokstein B. Grimm (2004) ArticleTitleThe gun4 gene is essential for cyanobacterial porphyrin metabolism FEBS Lett. 5 119–123

    Google Scholar 

  • R.D. Willows (2003) ArticleTitleBiosynthesis of chlorophylls from protoporphyrin IX Nat. Prod. Rep. 20 327–341 Occurrence Handle10.1039/b110549n Occurrence Handle1:CAS:528:DC%2BD3sXls1Klurs%3D Occurrence Handle12828371

    Article  CAS  PubMed  Google Scholar 

  • Wilson (2004) ArticleTitleDissection of maize kernel composition and starch production by candidate gene association Plant Cell 16 2719–2733 Occurrence Handle10.1105/tpc.104.025700 Occurrence Handle1:CAS:528:DC%2BD2cXptVShsrg%3D Occurrence Handle15377761

    Article  CAS  PubMed  Google Scholar 

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Sawers, R.J.H., Viney, J., Farmer, P.R. et al. The Maize Oil Yellow1 (Oy1) Gene Encodes the I Subunit of Magnesium Chelatase. Plant Mol Biol 60, 95–106 (2006). https://doi.org/10.1007/s11103-005-2880-0

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