Skip to main content

The Pathway from 5-Aminolevulinic Acid to Protochlorophyllide and Protoheme

  • Chapter
Chlorophylls and Bacteriochlorophylls

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 25))

Abstract

This chapter comprehensively surveys both the conversion of 5-aminolevulinic acid to protochlorophyllide in the Mg-porphyrin-synthesizing branch of tetrapyrrole biosynthesis and also the formation of protoheme in the iron-chelating branch. This can be considered as the middle and final stages of chlorophyll and heme formation, respectively: the final conversion of protochlorophyllide to chlorophyll is discussed by Rüdiger in Chapter14 (Rüdiger). This chapter reviews the many individual enzymatic steps in these conversions, including enzyme and gene structures and the expression as well as the regulation of these steps.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alawady AE and Grimm B (2005) Tobacco Mg protoporphyrin IX methyltransferase is involved in inverse activation of Mg porphyrin and protoheme synthesis. Plant J 41: 282–290

    PubMed  CAS  Google Scholar 

  • Alawady A, Reski R, Yaronskaya E and Grimm B (2005) Cloning and expression of the tobacco CHLM sequence encoding Mg protoporphyrin IX methyltransferase and its interaction with Mg chelatase. Plant Mol Biol 57: 679–691

    PubMed  CAS  Google Scholar 

  • Arnould S and Camadro JM (1998) The domain structure of protoporphyrinogen oxidase, the molecular target of diphenyl ethertype herbicides. Proc Natl Acad Sci USA 95: 10553–10558

    PubMed  CAS  Google Scholar 

  • Arnould S, Takahashi M and Camadro JM (1998) Stability of recombinant yeast protoporphyrinogen oxidase: effects of diphenyl ether-type herbicides and diphenyleneiodonium. Biochemistry 37: 12818–12828

    PubMed  CAS  Google Scholar 

  • Battersby, AR (1994) How nature builds the pigments of life: the conquest of Vitamin B12. Science 264: 1551–1557

    PubMed  CAS  Google Scholar 

  • Battersby AR, Fookes CJR, Gustafson-Potter KE, Matcham GWJ and McDonald E (1979a) Proof by synthesis that unrearranged hydroxymethylbilane is the product from deaminase and the substrate for cosynthetase in the biosynthesis of Uro'gen-III. J Chem Soc Chem Commun 1979: 1155–1158

    Google Scholar 

  • Battersby AR, Fookes CJR, Matcham GWJ and McDonald E (1979b) Order of assembly of the four pyrrole rings during biosynthesis of the natural porphyrins. J Chem Soc Chem Commun 1979: 539–541

    Google Scholar 

  • Battersby AR, Fookes CJR, Hart G, Matcham GWJ and Pandey PS (1983) Biosynthesis of porphyrins and related macrocycles. Part 21. The interaction of deaminase and its product (hydroxymethylbilane) and the relationship between deaminase and cosynthetase. J Chem Soc Perkin Trans: 3041–3047

    Google Scholar 

  • Berthold DA and Stenmark P (2003) Membrane-bound diiron carboxylate proteins. Ann Rev Plant Biol 54: 497–517

    CAS  Google Scholar 

  • Birchfield NB, Latli B and Casida JE (1998) Human protoporphyrinogen oxidase: Relation between the herbicide binding site and the flavin cofactor. Biochemistry 37: 6905–6910

    PubMed  CAS  Google Scholar 

  • Block MA, Tewari AK, Albrieux C, Maréchal E and Joyard J (2002) The plant S-adenosyl-L-methionine:Mg-protoporphyrin 1X methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur J Biochem 269: 240–248

    PubMed  CAS  Google Scholar 

  • Boese QF, Spano AJ, Li J and Timko MP (1991) Aminolevulinic acid dehydratase in pea (Pisum sarivum L.). J Biol Chem 266: 17060–17066

    PubMed  CAS  Google Scholar 

  • Bollivar DW and Beale SI (1995) Formation of the isocyclic ring of chlorophyll by isolated Chlamydomonas reinhardtii chloroplasts. Photosynth Res 43: 113–124

    CAS  Google Scholar 

  • Bollivar DW and Beale SI (1996) The chlorophyll biosynthetic enzyme Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase. Plant Physiol 112: 105–114

    PubMed  CAS  Google Scholar 

  • Bollivar DW, Jiang ZY, Bauer CE and Beale S (1994a) Heterologous expression of the bchM gene product from Rhodobacter capsulatus and demonstration that it encodes S-adenosyl-L-methionine: Mg-protoporphyrin 1X methyltransferase. J Bacteriol 176: 5290–5296

    CAS  Google Scholar 

  • Bollivar DW, Suzuki JY, Beatty JT, Dobrowolski JM and Bauer CE (1994b) Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. J Mol Biol 237: 622–640

    CAS  Google Scholar 

  • Breinig S, Kervinen J, Stith L, Wasson AS, Fairman R, Wlodawer A, Zdanov A and Jaffe EK (2003) Control of tetrapyrrole biosynthesis by alternate quaternary forms of porphobilinogen synthase. Nat Struct Biol 10: 757–763

    PubMed  CAS  Google Scholar 

  • Castelfranco PA, Weinstein JD, Schwarcz S, Pardo AD and Wezelman BE (1979) The Mg insertion step in chlorophyll biosynthesis. Arch Biochem Biophys 192: 592–598

    PubMed  CAS  Google Scholar 

  • Che F-S, Watanabe N, Iwano M, Inokuchi H, Takayama S, Yoshida S and Isogai A (2000) Molecular characterization and subcellular localization of protoporphyrinogen oxidase in spinach chloroplasts. Plant Physiol 124: 59–70

    PubMed  CAS  Google Scholar 

  • Chekounova E, Voronetskaya V, Papenbrock J, Grimm B and Beck CF (2001) Characterization of Chlamydomonas mutants defective in the H subunit of Mg-chelatase. Mol Gen Genet 266: 363–373

    CAS  Google Scholar 

  • Chereskin BM, Wong YS and Castelfranco PA (1982) In vitro synthesis of the chlorophyll isocyclic ring. Transformation of Mg-protoporphyrin IX and Mg-protoporphyrin IX monomethyl ester into magnesium-2,4-divinylpheoporphyrin a 5. Plant Physiol 70: 987–993

    PubMed  CAS  Google Scholar 

  • Cheung KM, Spencer P, Timko MP and Shoolingin-Jordan PM (1997) Characterization of a recombinant pea 5-aminolevulinic acid dehydratase and comparative inhibition studies with the Escherichia coli dehydratase. Biochemistry 36: 1148–1156

    PubMed  CAS  Google Scholar 

  • Choi KW, Han O, Lee HJ, Yun YC, Moon YH, Kim M, Kuk YI, Han SU and Guh JO (1998) Generation of resistance to the diphenyl ether herbicide, oxyfluorfen, via expression of the Bacillus subtilis protoporphyrinogen oxidase gene in transgenic tobacco plants. Biosci Biotechnol Biochem 62: 558–560

    CAS  Google Scholar 

  • Chow KS, Singh DP, Walker AR and Smith AG (1998) Two different genes encode ferrochelatase in Arabidopsis: Mapping, expression and subcellular targeting of the precursor proteins. Plant J 15: 531–541

    PubMed  CAS  Google Scholar 

  • Cornah JE, Roper JM, Singh DP and Smith AG (2002) 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.). Biochem J 362: 423–432

    PubMed  CAS  Google Scholar 

  • Crockett N, Alefounder PR, Battersby AR and Abell C (1991) Uroporphyrinogen III synthase: Studies on its mechanism of action molecular biology and biochemistry. Tetrahedron 47: 6003–6014

    CAS  Google Scholar 

  • Dailey HA, Daley TA, Wu CK, Medlock AE, Wang KF, Rose JP and Wang BC (2000) Ferrochelatase at the millennium: Structures, mechanisms and (2Fe-2S) clusters. Cell Mol Life Sci 57: 1909–1926

    PubMed  CAS  Google Scholar 

  • Duke SO, Becerril JM, Sherman TD, Lehnen LP and Matsumoto H (1991) Protoporphyrinogen oxidase-inhibiting herbicides. Weed Sci 39: 465–473

    CAS  Google Scholar 

  • Ellsworth RK and Dullaghan JP (1972) Activity and properties of S-adenosyl-L-methionine: Magnesium-protoporphyrin IX methyltransferase in crude homogenates from wheat seedling. Biochim Biophys Acta 268: 327–333

    PubMed  CAS  Google Scholar 

  • Ellsworth RK, Dullaghan JP and St. Pierre ME (1974) The reaction mechanism of S-adenosyl-L-methionine: Magnesium protoporphyrin IX methyltransferase of wheat. Photosynth 8: 375–383

    Google Scholar 

  • Erskine PT, Newbold R, Roper J, Coker A, Warren MJ, Shoolingin- Jordan PM, Wood SP and Cooper JB (1999) The Schiff base complex of yeast 5-aminolaevulinic acid dehydratase with laevulinic acid. Protein Sci 8: 1250–1256

    PubMed  CAS  Google Scholar 

  • Fodje MN, Hansson A, Hansson M, Olsen JG, Gough S, Willows RD and Al-Karadaghi S (2001) Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase. J Mol Biol 311: 111–122

    PubMed  CAS  Google Scholar 

  • Frankenberg N, Erskine PT, Cooper JB, Shoolingin-Jordan PM, Jahn D and Heinz DW (1999) High resolution crystal structure of a Mg2+-dependent porphobilinogen synthase. J Mol Biol 289: 591–602

    PubMed  CAS  Google Scholar 

  • Gibson KD, Neuberger A and Tait GH (1963) Studies on the biosynthesis of porphyrin and bacteriochlorophyll by Rhodopseudomonas spheriodes. 4. S-adenosylmethionine-magnesium protoporphyrin methyltransferase. Biochem J 88: 325–334

    PubMed  CAS  Google Scholar 

  • Gibson LCD and Hunter CN (1994) The bacteriochlorophyll biosynthesis gene, bchM, of Rhodobacter sphaeroides encodes S-adenosyl-L-methionine: Mg protoporphyrin IX methyltransferase. FEBS Lett 352: 127–130

    PubMed  CAS  Google Scholar 

  • Gibson LCD, Willows RD, Kannangara CG, von Wettstein D and Hunter CN (1995) Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: Reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli. Biochemistry 92: 1941–1944

    CAS  Google Scholar 

  • Gibson LCD, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M and Hunter CN (1996) A putative Mg chelatase subunit from Arabidopsis thaliana cv C24. Plant Physiol 111: 61–71

    PubMed  CAS  Google Scholar 

  • Goericke R and Repeta DJ (1993) Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean. Mar Ecol Prog Ser 101: 307–313

    CAS  Google Scholar 

  • Gorchein A (1972) Magnesium protoporphyrin chelatase activity in Rhodopseudomonas sphaeroides studies with whole cells. Biochem J 127: 97–106

    PubMed  CAS  Google Scholar 

  • Gorchein A, Gibson LCD and Hunter CN (1993) Gene expression and control of enzymes for synthesis of magnesium protoporphyrin monomethyl ester in Rhodobacter sphaeroides. Biochem Soc Trans 21: 201S

    PubMed  CAS  Google Scholar 

  • Gough SP, Petersen BO and Duus G (2000) Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97: 6908–6913

    PubMed  CAS  Google Scholar 

  • Grafe S, Saluz HP, Grimm B and Hanel F (1999) Mg-chelatase of tobacco: The role of the subunit CHL D in the chelation step of protoporphyrin IX. Proc Natl Acad Sci USA 96: 1941–1946

    PubMed  CAS  Google Scholar 

  • Guo R, Luo M and Weinstein JD (1998) Magnesium-chelatase from developing pea leaves. Characterization of a soluble extract from chloroplasts and resolution into three required protein fractions. Plant Physiol 116: 605–615

    CAS  Google Scholar 

  • Hansson A, Kannangara CG, von Wettstein D and Hansson M (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proc Natl Acad Sci USA 96: 1744–1749

    PubMed  CAS  Google Scholar 

  • Hansson A, Willows RD, Roberts TH and Hansson M (2002) Three 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

    PubMed  CAS  Google Scholar 

  • Hart GJ, and Battersby AR (1985) Purification and properties of uroporphyrinogen III synthase (co-synthase) from Euglena gracilis. Biochem J 232: 151–160

    PubMed  CAS  Google Scholar 

  • Hart GJ, Miller AD and Battersby AR (1987) Evidence that the pyrromethane cofactor of hydroxymethylbilane synthase (porphobilinogen deaminase) is bound through the sulfur atom of a cystein residue. Biochem J 252: 909–912

    Google Scholar 

  • Higuchi M and Bogorad L (1975) The purification and properties of uroporphyrinogen I synthase and uroporphyrinogen III cosynthase. Interaction between the enzymes. Ann NY Acad Sci 244: 401–418

    PubMed  CAS  Google Scholar 

  • Hinchigeri SB, Hundle B and Richards WR (1997) Demonstration that the BchH protein of Rhodobacter capsulatus activates S-adenosyl-L-methionine:magnesium protoporphyrin IX methyltransferase. FEBS Lett 407: 337–342

    PubMed  CAS  Google Scholar 

  • Hiriart J-B, Lehto K, Tyystjärvi, Junttila T and Aro E-M (2002) Suppression of a key gene involved in chlorophyll biosynthesis by means of virus-inducing gene silencing. Plant Mol Biol 50: 213–224

    PubMed  CAS  Google Scholar 

  • Hu G, Yalpani N, Briggs SP and Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10: 1095–1105

    PubMed  CAS  Google Scholar 

  • Hudson A, Carpenter R, Doyle S and Coen ES (1993) Olive: A key gene required for chlorophyll biosynthesis in Antirrhinum majus. EMBO J 12: 3711–3719

    PubMed  CAS  Google Scholar 

  • Ishikawa A, Okamoto H, Iwasaki Y and Asahi T (2001) A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J 27: 89–99

    PubMed  CAS  Google Scholar 

  • Jacobs JM and Jacobs NJ (1987) Oxidation of protoporphyrinogen to protoporphyrin, a step in chlorophyll and haem biosynthesis. Biochem J 244: 219–224

    PubMed  CAS  Google Scholar 

  • Jacobs JM and Jacobs NJ (1993) Porphyrin accumulation and export by isolated barley (Hordeum vulgare) plastids. Plant Physiol 101: 1181–1187

    PubMed  CAS  Google Scholar 

  • Jensen PE, Gibson LCD, Henningsen KW and Hunter CN (1996a) Expression 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

    CAS  Google Scholar 

  • Jensen PE, Willows RD, Petersen BL, Vothknecht UC, Stummann BM, Kannangara CG, von Wettstein D and Henningsen KW (1996b) Structural genes for Mg-chelatase subunits in barley: Xantha-f, -g and -h. Mol Gen Genet 250: 383–394

    CAS  Google Scholar 

  • Jensen PE, Gibson LCD and Hunter CN (1999a) ATPase 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: 127–134

    CAS  Google Scholar 

  • Jensen PE, Gibson LCD, Shephard F, Smith V and Hunter CN (1999b) Introduction of a new branchpoint in tetrapyrrole biosynthesis in Escherichia coli by co-expression of genes encoding the chlorophyll-specific enzymes magnesium chelatase and magnesium protoporphyrin methyltransferase. FEBS Lett 455: 349–354

    CAS  Google Scholar 

  • Jordan PM (1991) The biosynthesis of 5-aminolevulinic acid and its transformation into uroporphyrinogen III. In: Jordan PM (ed) Biosynthesis of Tetrapyrroles, New Comprehensive Biochemistry, Vol 19, pp 1–86. Elsevier, Amsterdam

    Google Scholar 

  • Jordan PM and Seehra JS (1979) The biosynthesis of uroporphyrinogen III. Order of assembly of the four porphobilinogen molecules in the formation of the tetrapyrrole ring. FEBS Lett 104: 364–366

    PubMed  CAS  Google Scholar 

  • Jordan PM and Warren MJ (1987) Evidence for a dipyrromethane cofactor at the catalytic site of Escherichia coli porphobilinogen deaminase. FEBS Lett 225: 87–92

    PubMed  CAS  Google Scholar 

  • Kaczor CM, Smith MW, Sangwan I and O'Brian MR (1994) Plant δ-aminolevulinic acid dehydratase. Plant Physiol 104: 1411–1417

    PubMed  CAS  Google Scholar 

  • Kjemtrup S, Sampson KS, Peele CG, Hguyen LV, Conkling MA, Thompson WF and Robertson D (1998) Gene silencing from plant DANN carried by a Geminivirus. Plant J 14: 91–100

    PubMed  CAS  Google Scholar 

  • Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R and Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: A key enzyme in haem and chlorophyll biosynthesis. EMBO J 23: 1720–1728.

    PubMed  CAS  Google Scholar 

  • Koncz C, Mayerhofer R, Koncz-Kalman Z, Nawrath C, Reiss B, Redei GP and Schell J (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J 9: 1337–1346

    PubMed  CAS  Google Scholar 

  • Kruse E, Mock HP and Grimm B (1995a) Coproporphyrinogen III oxidase from barley and tobacco—sequence analysis and initial expression studies. Planta 196: 796–803

    CAS  Google Scholar 

  • Kruse E, Mock H-P and Grimm B (1995b) Reduction of coproporphyrinogen oxidase level by antisense RNA synthesis leads to deregulated gene expression of plastid proteins and affects the oxidative defense system. EMBO J 14: 3712–3720

    CAS  Google Scholar 

  • Kruse E, Mock HP and Grimm B (1997) Isolation and characterisation of tobacco (Nicotiana tabacum) cDNA clones encoding proteins involved in magnesium chelation into protoporphyrin IX. Plant Mol. Biol 35: 1053–1056

    PubMed  CAS  Google Scholar 

  • Lecerof D, Fodje M, Hansson A, Hansson M and Al-Karadaghi S (2000) Structural and mechanistic basis of porphyrin metallation by ferrochelatase. J Mol Biol 297: 221–232

    PubMed  CAS  Google Scholar 

  • Lee HJ, Ball MD, Parham R and Rebeiz CA (1992) Chloroplast Biogenesis 65. Enzymic conversion of protoporphyrin IX to Mg-protoporphyrin IX in a subplastidic membrane fraction of cucumber etiochloroplasts. Plant Physiol 99: 1134–1140

    PubMed  CAS  Google Scholar 

  • Lee HJ, Lee SB, Chung JS, Han SU, Han O, Guh JO, Jeon JS, An G and Back K (2000) Transgenic rice plants expressing a Bacillus subtilis protoporphyrinogen oxidase gene are resistant to diphenyl ether herbicide oxyfluorfen. Plant Cell Physiol 41: 743–749

    PubMed  CAS  Google Scholar 

  • Lermontova I and Grimm B (2000) Overexpression of plastidic protoporphyrinogen IX oxidase leads to resistance to the diphenylether herbicide acifluorfen. Plant Physiol. 122: 75–84

    PubMed  CAS  Google Scholar 

  • Lermontova I, Kruse E, Mock H-P and Grimm B (1997) Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen 1X oxidase. Proc Natl Acad Sci USA 94: 8895–8900

    PubMed  CAS  Google Scholar 

  • Li X, Vollrath S, Nicholl DBG, Chilcott CE, Johnson MA, Ward ER and Law MD (2003) Development of protoporphyrinogen oxidase as an efficient selection marker for Agrobacterium tumefaciens-mediated transformation of maize. Plant Physiol 133: 736–747

    PubMed  CAS  Google Scholar 

  • Lim SI, Witty M, Wallace-Cook ADM, Hag LI and Smith AG (1994) Porphobilinogen deaminase is encoded by a single gene in Arabidopsis thaliana and is targeted to the chloroplasts. J Mol Biol 26: 863–872

    CAS  Google Scholar 

  • Lister R, Chew O, Rudhe C, Lee M-N and Whelan J (2001) Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett 506: 291–295

    PubMed  CAS  Google Scholar 

  • Louie GV, Brownlie PD, Lambert R, Cooper JB, Blundell TL, Wood SP, Malashkevich VN, Hadener A, Warren MJ and Schoolingin-Jordan PM (1996) The three-dimensional structure of Escherichia coli porphobilinogen deaminase at 1.76-Å resolution. Proteins 25: 48–78

    PubMed  CAS  Google Scholar 

  • Luo J and Lim CK (1993) Order of uroporphyrinogen III decarboxylation on incubation of porphobilinogen and uroporphyrinogen III with erythrocyte uroporphyrinogen decarboxylase. Biochem J 289: 529–532.

    PubMed  CAS  Google Scholar 

  • Luo M, Weinstein JD and Walker CJ (1999) Magnesium chelatase subunit D from pea: Characterization of the cDNA, heterologous expression of an enzymatically active protein and immunoassay of the native protein. Plant Mol Biol 41: 721–731

    PubMed  CAS  Google Scholar 

  • Martins BM, Grimm B, Mock H-P, Huber R and Messerschmidt A (2001) Crystal structure and substrate binding modeling of the uroporphyrinogen-III decarboxylase from Nicotiana tabacum. Implications for the catalytic mechanism. J Biol Chem 276: 44108–44116

    PubMed  CAS  Google Scholar 

  • Masuda T, Suzuki T, Shimada H, Ohta H and Takamiya K (2003) Subcellular localization of two types of ferrochelatase in cucumber. Planta 217: 602–609

    PubMed  CAS  Google Scholar 

  • Mathews MA, Schubert HL, Whitby FG, Alexander KJ, Schadick K, Bergonia HA, Phillips JD and Hill CP (2001). Crystal structure of human uroporphyrinogen III synthase. EMBO J 20: 5832–5839

    PubMed  CAS  Google Scholar 

  • Matringe M and Scalla R (1988) Effects of acifluorfen-methyl on cucumber cotyledons: Porphyrin accumulation. Pestic Biochem Physiol 32: 164–172

    CAS  Google Scholar 

  • Matringe M, Camadro JM, Joyard J and Douce R (1994) Localization of ferrochelatase activity within mature pea chloroplasts. J Biol Chem 269: 15010–15015

    PubMed  CAS  Google Scholar 

  • Matters GL and Beale SI (1995a) Structure and expression of the Chlamydomonas reinhardtii alad gene encoding the Chl biosynthetic enzyme, ä-aminolevulinic acid dehydratase (porphobilinogen synthase). Plant Mol Biol 27: 607–617

    CAS  Google Scholar 

  • Matters GL and Beale SI (1995b) Blue-light-regulated expression of genes for two early steps of chlorophyll biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 109: 471–479

    CAS  Google Scholar 

  • Miyamoto K, Tanaka R, Teramoto H, Masuda T, Tsuji H and Inokuchi H (1994) Nucleotide sequence of cDNA clones encoding ferrochelatase from barley and cucumber. Plant Physiol 105: 769–770

    PubMed  CAS  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis 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

    PubMed  CAS  Google Scholar 

  • Mock HP and Grimm B (1997) Reduction of uroporphyrinogen decarboxylase by antisense RNA expression affects activities of other enzymes involved in tetrapyrrole biosynthesis and leads to light-dependent necrosis. Plant Physiol 113: 1101–1112

    PubMed  CAS  Google Scholar 

  • Mock HP, Trainotti L, Kruse E and Grimm B (1995) Isolation, sequencing and expression of cDNA sequences encoding uroporphyrinogen decarboxylase from tobacco and barley. Plant Mol Biol 28: 245–256

    PubMed  CAS  Google Scholar 

  • Mock HP, Keetman U, Kruse E, Rank B and Grimm B (1998) Defense responses to tetrapyrrole-induced oxidative stress in transgenic plants with reduced uroporphyrinogen decarboxylase or coproporphyrinogen oxidase activity. Plant Physiol 116: 107–116

    CAS  Google Scholar 

  • Mock HP, Heller W, Molina A, Neubohn B, Sandermann H, Jr. and Grimm B (1999) Expression of uroporphyrinogen decarboxylase or coproporphyrinogen oxidase antisense RNA in tobacco induces pathogen defense responses conferring increased resistance to tobacco mosaic virus. J Biol Chem 274: 4231–4238

    PubMed  CAS  Google Scholar 

  • Molina A, Volrath S, Guyer D, Maleck K, Ryals J and Ward E (1999) Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J 17: 667–678

    PubMed  CAS  Google Scholar 

  • Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S and Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J 21: 6709–6720

    PubMed  CAS  Google Scholar 

  • Murphy MJ and Siegel LM (1973) Sirohaem and sirohydrochlorin. The basis for a new type of porphyrin-relatedf prosthetic group common to both assimilatory and dissimilatory sulfite reductases. J Biol Chem 248: 6911–6919

    PubMed  CAS  Google Scholar 

  • Nagata N, Tanaka R, Satoh S and Tanaka A (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17: 233–240

    PubMed  CAS  Google Scholar 

  • Nakayama M, Masuda T, Bando T, Yamagata H, Ohta H and Takamiya K-I (1998) Cloning and expression of the soybean chlH gene encoding a subunit of Mg-chelatase and localization of the Mg 2+ concentration-dependent ChlH protein within the chloroplast. Plant Cell Physiol 39: 275–284

    PubMed  CAS  Google Scholar 

  • Nasrulhaq-Boyce A, Griffiths WT and Jones OTG (1987) The use of continuous assays to characterize the oxidative cyclase that synthesizes the chlorophyll isocyclic ring. Biochem J 243: 23–29

    PubMed  CAS  Google Scholar 

  • Orsat B, Monfort A, Chatellard P and Stutz E (1992) Mapping and sequencing of an actively transcribed Euglena gracilis chloroplast gene (ccsA) homologous to the Arabidopsis thaliana nuclear gene cs (ch42). FEBS Lett 303: 181–184

    PubMed  CAS  Google Scholar 

  • Papenbrock J, Gräfe S, Kruse E, Hänel F and Grimm B (1997) Mg chelatase of tobacco: Identification of a Chl D cDNA sequence encoding a third subunit, analysis of the interaction of the three subunits with the yeast two-hybrid system, and reconstitution of the enzyme activity by co-expression of recombinant CHL D, CHL H and CHL I. Plant J 12: 981–990

    PubMed  CAS  Google Scholar 

  • Papenbrock J, Mock H-P, Kruse E and Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: Inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208: 264–273

    CAS  Google Scholar 

  • Papenbrock J, Mock H-P, Tanaka R, Kruse E and Grimm B (2000a) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122: 1161–1169

    CAS  Google Scholar 

  • Papenbrock J, Pfündel E, Mock H-P and Grimm B (2000b) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J 22: 155–164

    CAS  Google Scholar 

  • Papenbrock J, Mishra S, Mock H-P, Kruse E, Schmidt E-K, Petersmann A, Braun H-P and Grimm B (2001) Impaired expression of the plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic phenotype of transformed tobacco plants. Plant J 28: 41–50

    PubMed  CAS  Google Scholar 

  • Parham R and Rebeiz CA (1992) Chloroplast biogenesis: [4-Vinyl] chlorophyllide a reductase is a divinyl chlorophyllide a-specific, NADPH-dependent enzyme. Biochemistry 31: 8460–8464

    PubMed  CAS  Google Scholar 

  • Petersen BL, Jensen PE, Gibson LCD, Stummann BM, Hunter CN and Henningsen KW (1998) Reconstitution of an active magnesium chelatase enzyme complex from the bchl, -D, and -H gene products of the green sulfur bacterium Chlorobium vibrioforme expressed in Escherichia coli. J Bacteriol 180: 699–704

    PubMed  CAS  Google Scholar 

  • Petersen BL, Møller MG, Jensen PE and Henningsen KW (1999) Identification of the Xan-g gene and expression of the Mg-chelatase encoding genes Xan-f, -g and -h in mutant and wild type barley (Hordeum vulgare L). Hereditas 131: 165–170

    CAS  Google Scholar 

  • Pinta V, Picaud M, Reiss-Husson F and Astier C (2002) Rubrivivax gelantinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184: 746–753

    PubMed  CAS  Google Scholar 

  • Porra RJ and Lascelles J (1968) Studies on ferrochelatase: the enzymic formation of haem in proplastids, chloroplasts and plant mitochondria. Biochem J 108: 343–348

    PubMed  CAS  Google Scholar 

  • Porra RJ, Barnes R and Jones OTG (1973) The over-production of poprphyrins by semi-anaerobic yeast. Enzyme 16: 1–8

    PubMed  CAS  Google Scholar 

  • Porra RJ, Schäfer W, Katheder I and Scheer H (1995) The derivation of the oxygen atoms of the 131-oxo and 3-acetyl groups of bacteriochlorophyll a from water in Rhodobacter sphaeroides cells adapting from respiratory to photosynthetic conditions: evidence for an anaerobic pathway for the formation of isocyclic ring E. FEBS Lett 371: 21–24

    PubMed  CAS  Google Scholar 

  • Porra RJ, Urzinger M, Winkler J, Bubenzer C, and Scheer H (1998) Biosynthesis of the 3-acetyl and 131-oxo groups of bacteriochlorophyll a in the facultative aerobic bacterium, Rhodovulum sulfidophilum: The presence of both oxygenase and hydratase pathways for isocyclic ring formation. Eur J Biochem 252: 185–191

    Google Scholar 

  • Randolph-Anderson BL, Sato R, Johnson AM, Harris EH, Hauser CR, Oeda K, Ishige F, Nishio S, Gillham NW and Boynton JE (1998) Isolation and characterization of a mutant protoporphyrinogen oxidase gene from Chlamydomonas reinhardtii conferring resistance to porphyric herbicides. Plant Mol Biol 38: 839–859

    PubMed  CAS  Google Scholar 

  • Rebeiz CA, Wu SM, Kuhagja M, Daniell H and Perkins EJ (1983) Chlorophyll a biosynthetic routes and chlorophyll a chemical heterogeneity in plants. Mol Cell Biochem 57: 97–125

    PubMed  CAS  Google Scholar 

  • Rimington C and Miles PA (1951) A study of porphyrins excreted in the urine by a case of congenital porphyria. Biochem J 50: 202–206

    PubMed  CAS  Google Scholar 

  • Rissler HM, Collakova E, DellaPenna D, Whelan J and Pogson BJ (2002) Chlorophyll biosynthesis. Expression of a second Chl I gene of magnesium chelatase in Arabidopsis supports only limited chlorophyll synthesis. Plant Physiol 128: 770–779

    PubMed  CAS  Google Scholar 

  • Roper JM and Smith AG (1997) Molecular localization of ferrochelatase in higher plant chloroplasts. Eur J Biochem 246: 32–37

    PubMed  CAS  Google Scholar 

  • Santana MA, Pihakaski-Maunsbach K, Sandal N, Marcker KA and Smith AG (1998) Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol 116: 1259–1269

    PubMed  CAS  Google Scholar 

  • Scalla R, Matringe M, Camadro JM and Labbe P (1990) Recent advances in the mode of action of diphenyl ether and related herbicides. Z Naturforsch 45c: 503–511

    Google Scholar 

  • Schaumburg A and Schneider-Poetsch HAW (1992) Characterization of plastid 5-aminolevulinate dehydratase (ALAD; EC 4.2.1.24) from spinach (Spinacia oleracea) by sequencing and comparison with non-plant ALAD enzymes. Z Naturforsch 47c: 77–84

    Google Scholar 

  • Schubert HL, Raux E, Matthews MA, Phillips JD, Wilson KS, Hill CP and Warren MJ (2002) Structural diversity in metal ion chelation and the structure of uroporphyrinogen III synthase. Biochem Soc Trans 30: 595–600

    PubMed  CAS  Google Scholar 

  • Senior NM, Brocklehurst K, Cooper JB, Wood SP, Erskine P, Shoolingin-Jordan PM, Thomas PG and Warren MJ (1996) Comparative studies on the 5-aminolaevulinic acid dehydratases from Pisum sativum, Escherichia coli and Saccharomyces cerevisiae. Biochem J 320: 401–412

    PubMed  CAS  Google Scholar 

  • Shalygo NV, Averina NG, Grimm B and Mock H-P (1997) Influence of cesium on tetrapyrrole biosynthesis in etiolated and greening barley leaves. Physiol Plant 99: 160–168

    CAS  Google Scholar 

  • Shalygo NV, Mock H-P, Averina NG and Grimm B (1998) Photodynamic action of uroporphyrin and protochlorophyllide in greening barley leaves treated with cesium chloride. J Photochem Photobiol 42: 151–158

    CAS  Google Scholar 

  • Singh DP, Cornah JE, Hadingham S and Smith AG (2002) Expression analysis of the two ferrochelatase genes in Arabidopsis in different tissues and under stress conditions reveals their different roles in haem biosynthesis. Plant Mol Biol 50: 773–788

    PubMed  CAS  Google Scholar 

  • Smith AG (1988) Subcellular localization of two porphyrin-synthesis enzymes in Pisum sativum (pea) and Arum (cuckoo-pint) species. Biochem J 249: 423–428

    PubMed  CAS  Google Scholar 

  • Smith AG, Marsh O and Elder GH (1993) Investigation of the subcellular location of the tetrapyrrole-biosynthesis enzyme coproporphyrinogen oxidase in higher plants. Biochem J 292: 503–508

    PubMed  CAS  Google Scholar 

  • Smith AG, Santana MA, Wallace-Cook AD, Roper JM and Labbe-Bois R (1994) Isolation of cDNA encoding chloroplast ferrochelatase from Arabidopsis thaliana by functional complementation of a yeast mutant. J Biol Chem 259: 13405–13413

    Google Scholar 

  • Smith CA, Suzuki JY and Bauer CE (1996) Cloning and characterization of the chlorophyll biosynthesis gene chlM from Synechocystis PCC 6803 by complemention of a bacteriochlorophyll biosynthesis mutant of Rhodobacter capsulatus. Plant Mol Biol 30: 1307–1314

    PubMed  CAS  Google Scholar 

  • Stark WM, Hawker CJ, Hart GJ, Philippides A, Petersen PM, Lewis JD, Leeper FJ and Battersby AR (1993) Biosynthesis of porphyrins and related macrocycles. Part 40. Synthesis of a spiro-lactam related to the proposed spiro-intermediate for porphyrin biosynthesis: Inhibition of cosynthetase. J Chem Soc Perkin Trans I 1993: 2875–2891

    Google Scholar 

  • Suzuki JY and Bauer CE (1995) Altered monovinyl and divinyl protochlorophyllide pools in bchJ mutants of Rhodobacter capsulatus. Possible monovinyl substrate discrimination of light-independent protochlorophyllide reductase. J Biol Chem 270: 3732–3740

    PubMed  CAS  Google Scholar 

  • Suzuki T, Masuda T, Inokuchi H, Shimada H, Ohta H and Takamiya K-I (2000) Overexpression, enzymatic properties and tissue localization of a ferrochelatase of cucumber. Plant Cell Physiol 41: 192–199

    PubMed  CAS  Google Scholar 

  • Suzuki T, Masuda T, Singh DP, Tan F-C, Tohru T, Shimada H, Ohta H, Smith AG and Takamiya K-I (2002) Two types of ferrochelatase in photosynthetic and non- photosynthetic tissues of cucumber; their difference in phylogeny, gene expression and localization. J Biol Chem 277: 4731–4737

    PubMed  CAS  Google Scholar 

  • Tripathy BC and Rebeiz CA (1988) Chloroplast biogenesis 60: Conversion of divinyl protochlorophyllide to monovinyl protochlorophyllide in green(ing) barley, a dark monovinyl/light divinyl plant species. Plant Physiol 87: 89–94

    PubMed  CAS  Google Scholar 

  • Walker CJ and Weinstein JD (1991) In vitro assay of the chlorophyll biosynthetic enzyme Mg-chelatase: Resolution of the activity into soluble and membrane-bound fractions. Biochemistry 88: 5789–5793

    CAS  Google Scholar 

  • Walker CJ and Willows RD (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327: 321–333

    PubMed  CAS  Google Scholar 

  • Walker CJ, Castelfranco PA and Whyte BJ (1991) Synthesis of divinyl protochlorophyllide. Enzymological properties of the Mg-protoporphyrin 1X monomethyl ester oxidative cyclase system. Biochem J 276: 691–697

    PubMed  CAS  Google Scholar 

  • Watanabe N, Che F-S, Iwano M, Takayama S, Nakano T, Yoshida S and Isogai A (1998) Molecular characterization of photomixotrophic tobacco cells resistant to protoporphyrinogen oxidase inhibiting herbicides. Plant Physiol 118: 751–758

    PubMed  CAS  Google Scholar 

  • Watanabe N, Che F-S, Iwano M, Takayama S, Yoshida S and Isogai A (2001) Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem 276: 20474–20481

    PubMed  CAS  Google Scholar 

  • Watanabe N, Takayama S, Yoshida S, Isogal A and Fang-Sik C (2002) Resistance to protoporphyrinogen oxidase-inhibiting compound S23142 from overproduction of mitochondrial protoporphyrinogen oxidase by gene amplification in photomixotrophic tobacco cells. Biosci Biotechnol Biochem 66: 1799–1805

    PubMed  CAS  Google Scholar 

  • Whitby FG, Phillips JD, Kushner JP and Hill CP (1998) Crystal structure of human uroprophyrinogen decarboxylase. EMBO J 17: 2463–2471

    PubMed  CAS  Google Scholar 

  • Whyte BJ, Vijayan P and Castelfranco PA (1992) In vitro synthesis of protochlorophyllide: effects of Mg2+ and other cations on the reconstituted (oxidative) cyclase. Plant Physiol Biochem 30: 279–284

    CAS  Google Scholar 

  • Willows RD and Beale SI (1998) Heterologous expression of the Rhodobacter capsulatus bchI, -D, and -H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme. J Biol Chem 273: 34206–34213

    PubMed  CAS  Google Scholar 

  • Willows RD, Gibson LCD, Kanangara CG, Hunter CN and von Wettstein D (1996) Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides. Eur J Biochem 235: 438–445

    PubMed  CAS  Google Scholar 

  • Witty M, Wallace-Cook ADM, Albrecht H, Spano AJ, Michel H, Shabanowitz J, Hunt DF, Timko MP and Smith AG (1993) Structure and expression of chloroplast-localized porphobilinogen deaminase from pea (Pisum sativum L.) isolated by redundant polymerase chain reaction. Plant Physiol 103: 139–147

    PubMed  CAS  Google Scholar 

  • Wong Y-S and Castelfranco PA (1984) Properties of the Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase system. Plant Physiol 79: 730–733

    Google Scholar 

  • Wong Y-S, Castelfranco PA, Goff DA and Smith KM (1985) Intermediates in the formation of the chlorophyll isocyclic ring. Plant Physiol 79: 725–729

    PubMed  CAS  Google Scholar 

  • Wu CK, Dailey HA, Rose JP, Burden A, Sellers VM and Wang BC (2001) The 2.0 A structure of human ferrochelatase, the terminal enzyme of heme biosynthesis. Nat Struct Biol 8: 156–160

    PubMed  CAS  Google Scholar 

  • Zheng CC, Porat R, Lu P and O'Neill SD (1998) PNZIP is a novel mesophyll-specific cDNA that is regulated by phytochrome and the circadian rhythm and encodes a protein with a leucine zipper motif. Plant Physiol 116: 27–35

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2006 Springer

About this chapter

Cite this chapter

Yaronskaya, E., Grimm, B. (2006). The Pathway from 5-Aminolevulinic Acid to Protochlorophyllide and Protoheme. In: Grimm, B., Porra, R.J., Rüdiger, W., Scheer, H. (eds) Chlorophylls and Bacteriochlorophylls. Advances in Photosynthesis and Respiration, vol 25. Springer, Dordrecht. https://doi.org/10.1007/1-4020-4516-6_13

Download citation

Publish with us

Policies and ethics