Amino Acids

, Volume 30, Issue 2, pp 127–142

Histidine biosynthesis in plants

  • A. Stepansky
  • T. Leustek
Review Article

Summary.

The study of histidine metabolism has never been at the forefront of interest in plant systems despite the significant role that the analysis of this pathway has played in development of the field of molecular genetics in microbes. With the advent of methods to analyze plant gene function by complementation of microbial auxotrophic mutants and the complete analysis of plant genome sequences, strides have been made in deciphering the histidine pathway in plants. The studies point to a complex evolutionary origin of genes for histidine biosynthesis. Gene regulation studies have indicated novel regulatory networks involving histidine. In addition, physiological studies have indicated novel functions for histidine in plants as chelators and transporters of metal ions. Recent investigations have revealed intriguing connections of histidine in plant reproduction. The exciting new information suggests that the study of plant histidine biosynthesis has finally begun to flower.

Keywords: Histidine – Biosynthesis – Plants 

Abbreviations

PRPP

phosphoribosylpyrophosphate

PRATP

N′-5′-phosphoribosyl-ATP

ATP-PRT

N′-5′-phosphoribosyl-ATP transferase

PR-AMP

N′-5′-phosphoribosyl-AMP

5′-ProFAR or BBMII

N′-[(5′-phosphoribosyl)-formimino]5-aminoimidazole-4-carboxamide-ribonucleotide

PRA-PH

phosphoribosyl ATP pyrophosphohydrolase

PRA-CH

phosphoribosyl-AMP cyclohydrolase

5′-PRFAR or BBMIII

N′-[(5′-phosphoribulosyl)-formimino]-5-aminoimidazole-4-carboxamide-ribonucleotide

IGP

imidazoleglycerol-phosphate

AICAR

5′-amino-4-carboxamide ribonucleotide

IGPD

imidazoleglycerol-phosphate dehydratase

IAP

imidazole acetolphosphate

HOL-P

L-histidinolphosphate

HOL

L-histidinol

HAL

L-histidinal

AIR

aminoimidazole ribotide

HMP

hydroxymethylpyrimidine

THF

tetrahydrofolate

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References

  1. Albani, D, Hammond-Kosack, MCU, Smith, C, Conlan, S, Colot, V, Holdsworth, M, Bevan, MW 1997The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes the GCN4-like motif in the bifactorial endosperm box of prolamin genes.Plant Cell9171184CrossRefPubMedGoogle Scholar
  2. Alifano, P, Fani, R, Lio, P, Lazcano, A, Bazzicalupo, M, Carlomagno, MS, Bruni, CB 1996Histidine biosynthetic pathway and genes: structure, regulation, and evolution.Microbiol Rev604469PubMedGoogle Scholar
  3. Allen, S, Zilles, JL, Downs, DM 2002Metabolic flux in both the purine mononucleotide and histidine biosynthetic pathways can influence synthesis of the hydroxymethyl pyrimidine moiety of thiamine in Salmonella enterica.J Bacteriol18461306137CrossRefPubMedGoogle Scholar
  4. Ames, BN, Garry, B, Herzenberg, LA 1960The genetic control of the enzymes of histidine biosynthesis in Salmonella typhimurium.J Gen Microbiol22369378PubMedGoogle Scholar
  5. Ames, BN, Hartman, PE, Jacob, F 1963Chromosomal alterations affecting the regulation of histidine biosynthetic enzymes in Salmonella.J Mol Biol72342PubMedGoogle Scholar
  6. Anton, DN 1968Histidine regulatory mutants in Salmonella typhimurium. V. Two new classes of histidine regulatory mutants.J Mol Biol33533546CrossRefPubMedGoogle Scholar
  7. Arndt, KT, Styles, C, Fink, GR 1987Multiple global regulators control HIS4 transcription in yeast.Science237874880PubMedGoogle Scholar
  8. Beckler, GS, Reeve, JN 1986Conservation of primary structure in the hisI gene of the archaeabacterium, Methanococcus vannielli, the eubacterium Escherichia coli, and the eucaryote Saccharomyces cerevisiae.Mol Gen Genet204133140CrossRefPubMedGoogle Scholar
  9. Brilli, M, Fani, R 2004aThe origin and evolution of eucaryal HIS7 genes: from metabolon to bifunctional proteins?Gene339149160CrossRefGoogle Scholar
  10. Brilli, M, Fani, R 2004bMolecular evolution of hisB genes.J Mol Evol58225237CrossRefGoogle Scholar
  11. Bult, CJ, White, O, Olsen, GJ, Zhou, L, Fleischmann, RD, Sutton, GG, Blake, JA, FitzGerald, LM, Clayton, RA, Gocayne, JD, Kerlavage, AR, Dougherty, BA, Tomb, JF, Adams, MD, Reich, CI, Overbeek, R, Kirkness, EF, Weinstock, KG, Merrick, JM, Glodek, A, Scott, JL, Geoghagen, NS, Venter, JC 1996Complete genome sequence of the methanogenic archaeon, Methanococcus jannaschii.Science27310581073PubMedGoogle Scholar
  12. Carsiotis, M, Jones, RF 1974Cross-pathway regulation: tryptophan-mediated control of histidine and arginine biosynthetic enzymes in Neurospora crassa.J Bacteriol119889892PubMedGoogle Scholar
  13. Chiariotti, L, Nappo, AG, Carlomagno, MS, Bruni, CB 1986Gene structure in the histidine operon of Escherichia coli: identification and nucleotide sequence of the hisB gene.Mol Gen Genet2024247CrossRefPubMedGoogle Scholar
  14. Dawson RMC, Elliott DC, Elliott WH, Jones KM (1986) Data for biochemical research, 3rd ed. Clarendon Press, OxfordGoogle Scholar
  15. DeFraia C, Leustek T (2004) Functional genomics study in Arabidopsis thaliana of histidine biosynthesis. The Rutgers Scholar: An Electronic Bulletin of Undergraduate Research, vol 6 (http://rutgersscholar.rutgers.edu/index.html)
  16. Denis, V, Boucherie, H, Monribot, C, Daignan-Fornier, B 1998Role of the myb-like protein Bas1p in Saccharomyces cerevisiae: a proteome analysis.Mol Microbiol30557566CrossRefPubMedGoogle Scholar
  17. Ehrenshaft, M, Daub, ME 2001Isolation of PDX2, a second novel gene in the pyridoxine biosynthesis pathway of eukaryotes, archaebacteria, and a subset of eubacteria.J Bacteriol18333833390CrossRefPubMedGoogle Scholar
  18. El Malki, FE, Frankard, V, Jacobs, M 1998Molecular cloning and expression of a cDNA sequence encoding histidinol phosphate aminotransferase from Nicotiana tabacum.Plant Mol Biol3710131022CrossRefPubMedGoogle Scholar
  19. El Malki, FE, Jacobs, M 2001Molecular characterization and expression study of a histidine auxotrophic mutant (his1) of Nicotiana plumbaginifolia.Plant Mol Biol45191199CrossRefPubMedGoogle Scholar
  20. Fani, R, Alifano, P, Allotta, G, Bazzicalupo, M, Carlomagno, MS, Gallori, E, Rivellini, F, Polsinelli, M 1993The histidine operon of Azospirillum brasilense: organization, nucleotide sequence and functional analysis.Res Microbiol144187200CrossRefPubMedGoogle Scholar
  21. Fink, GR, Klopotowski, T, Ames, BN 1967Histidine regulatory mutants in Salmonella typhimurium. IV. A positive selection for polar histidine-requiring mutants from histidine operator constitutive mutants.J Mol Biol308195PubMedGoogle Scholar
  22. Fujimori, K, Ohta, D 1998aIsolation and characterization of a histidine biosynthetic gene in Arabidopsis encoding a polypeptide with two separate domains for phosphoribosyl-ATP pyrophosphohydrolase and phosphoribosyl-AMP cyclohydrolase.Plant Physiol118275283CrossRefGoogle Scholar
  23. Fujimori, K, Ohta, D 1998bAn Arabidopsis cDNA encoding a bifunctional glutamine amidotransferase/cyclase suppresses the histidine auxotrophy of Saccharomyces cerevisiae HIS7 mutant.FEBS Lett428229234CrossRefGoogle Scholar
  24. Fujimori, K, Tada, S, Kanai, S, Ohta, D 1998Molecular cloning and characterization of the gene encoding N′-[(5′-phosphoribosyl)-formino]-5-aminoimidazole-4-carboxamide ribonucleotide (BBM II) isomerase from Arabidopsis thaliana.Mol Gen Genet259216223PubMedGoogle Scholar
  25. Galperin, MY, Koonin, EV 1997A diverse superfamily of enzymes with ATP-dependent carboxylate-amine/thiol ligase activity.Protein Sci626392643PubMedGoogle Scholar
  26. Gantt, JS, Baldauf, SL, Calie, PJ, Weeden, NF, Palmer, JD 1991Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron.EMBO J1030733078PubMedGoogle Scholar
  27. Ghislain, M, Frankard, V, Vandenbossche, D, Mattews, BF, Jacobs, M 1994Molecular analysis of the aspartate kinase-homoserine dehydrogenase gene from Arabidopsis thaliana.Plant Mol Biol24835851CrossRefPubMedGoogle Scholar
  28. Guyer, D, Patton, D, Ward, E 1995Evidence for cross-pathway regulation of metabolic gene expression in plants.Proc Natl Acad Sci USA9249975000PubMedGoogle Scholar
  29. Hartman, PE 1956Linked loci in the control of consecutive steps in the primary pathway of histidine synthesis in Salmonella typhimurium.Carnegie Inst Wash Publ6123562Google Scholar
  30. Hinnebusch, AG 1992Transcriptional and translational regulation of gene expression in the general control of amino acid biosynthesis in Saccharomyces serevisiae.Prog Nucleic Acid Res Mol Biol38195240Google Scholar
  31. Holmes, WB, Appling, DR 2002Cloning and characterization of methenyltetrahydrofolate synthetase from Saccharomyces cerevisiae.J Biol Chem2772020520213PubMedGoogle Scholar
  32. Ingle, RA, Mugford, ST, Rees, JD, Campbell, MM, Smith, AC 2005Constitutively high expression of the histidine biosynthetic pathway contributes to nickel tolerance in hyperaccumulator plants.Plant Cell17118CrossRefGoogle Scholar
  33. Joho, M, Inouhe, M, Tohoyama, H, Murayama, T 1990A possible role of histidine in a nickel resistant mechanism in Saccharomyces cerevisiae.FEMS Microbiol Lett66333338CrossRefGoogle Scholar
  34. Kereb, L, Krämer, U 2003The role of free histidine in xylem loading of nickel in Alyssum lesbiacum and Brassica juncea.Plant Physiol131716724Google Scholar
  35. Kheirolomoom, A, Mano, J, Nagai, A, Ogawa, A, Iwasaki, G, Ohta, D 1994Steady-state kinetics of cabbage histidinol dehydrogenase.Arch Biochem Biophys312493500CrossRefPubMedGoogle Scholar
  36. Klem, TJ, Davisson, VJ 1993Imidazole glycerol phosphate synthase: the glutamine amidotransferase in histidine biosynthesis.Biochemistry3251775186CrossRefPubMedGoogle Scholar
  37. Krämer, U, Cotter-Howells, JD, Chanock, J, Baker, A, Smith, JAS 1996Free histidine as a metal chelator in plants that accumulate nickel.Nature379635638CrossRefGoogle Scholar
  38. Le Coq, , Fillinger, S, Aymerich, S 1999Histidinol phosphate phosphatase, catalyzing the penultimate step of the histidine biosynthesis pathway, is encoded by ytvP (hisJ) in Bacillus subtilis.J Bacteriol1832773280Google Scholar
  39. Lescot, M, Díhais, P, Thijs, G, Marchal, K, Moreau, Y, Van de Peer, Y, Rouzí, P, Rombauts, S 2002PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequence.Nucleic Acids Res30325327CrossRefPubMedGoogle Scholar
  40. Liao, MT, Hedley, MJ, Woolley, DJ, Brooks, RR, Nichols, MA 2000Copper uptake and translocation in chicory (Cichorium intybus L. cv Grasslands Puna) and tomato (Lycopersicon esculentum Mill. cv Rondy) plants growth in NFT system. II. The role of nicotianamine and histidine in xylem sap copper transport.Plant Soil223243252CrossRefGoogle Scholar
  41. Mano, J, Hatano, M, Koizumi, S, Tada, S, Hashimoto, M, Scheidegger, A 1993Purification and properties of a monofunctional imidazoleglycerol-phosphate dehydratase from wheat.Plant Physiol103733739PubMedGoogle Scholar
  42. Mauri, I, Maddaloni, M, Lohmer, S, Motto, M, Salamini, F, Tompson, R, Martegani, E 1993Functional expression of the transcription activator Opaque-2 of Zea mays in transformed yeast.Mol Gen Genet241319326CrossRefPubMedGoogle Scholar
  43. Miflin BJ (1980) Histidine biosynthesis. In: Stumpf PK, Conn EE (eds) The biochemistry of plants: a comprehensive treatise, vol 5: Amino acids and derivatives. Academic Press, New York, pp 533–541Google Scholar
  44. Muller, M, Knudsen, S 1993The nitrogen response of a barley C-hordein promoter is controlled by positive and negative regulation of the GCN4 and endosperm box.Plant J4343355CrossRefPubMedGoogle Scholar
  45. Nagai, A, Scheidegger, A 1991Purification and characterization of histidinol dehydrogenase from cabbage.Arch Biochem Biophys284127132CrossRefPubMedGoogle Scholar
  46. Nagai, A, Suzuki, K, Ward, E, Moyer, M, Hashimoto, M, Mano, J, Ohta, D, Scheidegger, A 1992Overexpression of plant histidinol dehydrogenase using a baculovirus expression vector system.Arch Biochem Biophys295235239CrossRefPubMedGoogle Scholar
  47. Natarajan, K, Meuer, MR, Jackson, BM, Slade, D, Roberts, C, Hinnebusch, AG, Marton, MJ 2001Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast.Mol Cell Biol2143474368CrossRefPubMedGoogle Scholar
  48. Noctor, G, Novitskaya, L, Lea, PJ, Foyer, CH 2002Co-ordination of leaf minor amino acid contents in crop species: significance and interpretation.J Exp Bot53939945PubMedGoogle Scholar
  49. Noutoshi, Y, Ito, T, Shinozaki, K 2005Albino and Pale Green 10 encodes BBMII isomerase involved in the histidine biosynthesis in Arabidopsis thaliana.Plant Cell Physiol4611651172CrossRefPubMedGoogle Scholar
  50. Ohta, D, Fujimori, K, Mizutani, M, Nakayama, Y, Kunpaisal-Hashimoto, R, Munzer, S, Kozaki, A 2000Molecular cloning and characterization of ATP-phosphoribosyl transferase from Arabidopsis, a key enzyme in the histidine biosynthetic pathway.Plant Physiol122907914CrossRefPubMedGoogle Scholar
  51. Pearce, DA, Sherman, F 1999Toxicity of copper, cobalt and nickel salts is dependent on histidine metabolism in the yeast Saccharomyces cerevisiae.J Bacteriol18147744779PubMedGoogle Scholar
  52. Pendyala, L, Wellman, A 1975Effect of histidine on purine nucleotide synthesis and utilization in Neurospora crassa.J Bacteriol1247885PubMedGoogle Scholar
  53. Persans, M, Yan, X, Smith, R, Salt, DE 1998Cloning of two cDNAs from the Ni hyperaccumulator Thlaspi goesingense: histidinol dehydrogenase and imidazoleglycerol-phosphate dehydratase, two enzymes in the histidine biosynthetic pathway.Plant Physiol117332Google Scholar
  54. Persans, MW, Yan, X, Patnoe, JM, Krämer, U, Salt, DE 1999Molecular dissection of the role of histidine in nickel hyperaccumulation in Thlaspi goesingense (Halacsy).Plant Physiol12111171126CrossRefPubMedGoogle Scholar
  55. Radwansky, ER, Last, RL 1995Tryptophan biosynthesis and metabolism: biochemical and molecular genetics.Plant Cell7921934Google Scholar
  56. Salt, DE, Prince, RC, Baker, AJM, Raskin, I, Pickering, IJ 1999Zinc ligand in the metal hyperaccumulator Thlaspi caerulescens as determined using x-ray absorption spectroscopy.Environ Sci Technol33713717CrossRefGoogle Scholar
  57. Sasaki, T, Matsumoto, T, Yamamoto, K, Sakata, K, Baba, T, Katayose, Y, Wu, J, Niimura, Y, Cheng, Z, Nagamura, Y, Antonio, BA, Kanamori, H, Hosokawa, S, Masukawa, M, Arikawa, K, Chiden, Y, Hayashi, M, Okamoto, M, Ando, T, Aoki, H, Arita, K, Hamada, M, Harada, C, Hijishita, S, Honda, M, Ichikawa, Y, Idonuma, A, Iijima, M, Ikeda, M, Ikeno, M, Ito, S, Ito, T, Ito, Y, Ito, Y, Iwabuchi, A, Kamiya, K, Karasawa, W, Katagiri, S, Kikuta, A, Kobayashi, N, Kono, I, Machita, K, Maehara, T, Mizuno, H, Mizubayashi, T, Mukai, Y, Nagasaki, H, Nakashima, M, Nakama, Y, Nakamichi, Y, Nakamura, M, Namiki, N, Negishi, M, Ohta, I, Ono, N, Saji, S, Sakai, K, Shibata, M, Shimokawa, T, Shomura, A, Song, J, Takazaki, Y, Terasawa, K, Tsuji, K, Waki, K, Yamagata, H, Yamane, H, Yoshiki, S, Yoshihara, R, Yukawa, K, Zhong, H, Iwama, H, Endo, T, Ito, H, Hahn, JH, Kim, HI, Eun, MY, Yano, M, Jiang, J, Gojobori, T 2002The genome sequence and structure of rice chromosome.Nature420312316CrossRefPubMedGoogle Scholar
  58. Silbert, DF, Fink, GR, Ames, BN 1966Histidine regulatory mutants in Salmonella typhimurium. III. A class of regulatory mutants deficient in tRNA for histidine.J Mol Biol22335347CrossRefPubMedGoogle Scholar
  59. Springer, C, Kunzler, M, Balmelli, T, Braus, GH 1996Amino acid and adenine cross-pathway regulation act through the same 5′-TGACTC-3′ motif in the yeast HIS7 promoter.J Biol Chem2712963729643PubMedGoogle Scholar
  60. Staples, MA, Houston, LL 1979Proteolytic degradation of imidazoleglycerolphosphate dehydratase-histidinol phosphatase from Salmonella typhimurium and the isolation of a resistant bifunctional core enzyme.J Biol Chem25413951401PubMedGoogle Scholar
  61. Tada, S, Hatano, M, Nakayama, Y, Volrath, S, Guyer, D, Ward, E, Ohta, D 1995Insect cell expression of recombinant imidazoleglycerolphosphate dehydratase of Arabidopsis and wheat and inhibition by triazole herbicides.Plant Physiol109153159CrossRefPubMedGoogle Scholar
  62. Tada, S, Volrath, S, Guyer, D, Scheidegger, A, Ryals, J, Ohta, D, Ward, E 1994Isolation and characterization of cDNAs encoding imidazoleglycerolphosphate dehydratase from Arabidopsis.Plant Physiol105579583CrossRefPubMedGoogle Scholar
  63. Tice-Baldwin, K, Fink, GR, Arndt, KT 1989BAS1 has a Myb motif and activates HIS4 transcription only in combination with BAS2.Science246931935PubMedGoogle Scholar
  64. Wapnir, RA, Khani, DE, Bayne, MA, Lifshitz, F 1983Absorption of zinc by the rat ileum: effects of histidine and other low-molecular-weight ligands.J Nutr11313461354PubMedGoogle Scholar
  65. Wiater, A, Krajewska-Grynkiewicz, K, Klopotowski, T 1971Histidine biosynthesis and its regulation in higher plants.Acta Biochim Polon18299307PubMedGoogle Scholar
  66. Winkler ME (1987) Biosynthesis of histidine. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol 1. American Society for Microbiology, Washington, DC, pp 395–411Google Scholar
  67. Wolter, FP, Fritz, CC, Willmitzer, L, Schell, J, Schreier, PH 1988rbcS genes in Solanum tuberosum: conservation of transit peptide and exon shuffling during evolution.Proc Natl Acad Sci USA85846850PubMedGoogle Scholar
  68. Wycisk, K, Kim, EJ, Schroeder, JI, Krämer, U 2004Enhancing the first enzymatic step in the histidine biosynthesis pathway increases the free histidine pool and nickel tolerance in Arabidopsis thaliana.FEBS Lett578128134CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2006

Authors and Affiliations

  • A. Stepansky
    • 1
  • T. Leustek
    • 1
  1. 1.Biotechnology Center for Agriculture and the Environment, Rutgers UniversityNew BrunswickU.S.A.

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