An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Olaf Czarnecki
  • Boris Hedtke
  • Michael Melzer
  • Maxi Rothbart
  • Andreas Richter
  • Yvonne Schröter
  • Thomas Pfannschmidt
  • Bernhard Grimm

Research Organisations

External Research Organisations

  • Institute of Agricultural and Urban Ecological Projects at Humboldt University of Berlin (IASP)
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Details

Original languageEnglish
Pages (from-to)4476-91
Number of pages16
JournalThe plant cell
Volume23
Issue number12
Publication statusPublished - Dec 2011

Abstract

5-Aminolevulinic acid (ALA) is the universal precursor for tetrapyrrole biosynthesis and is synthesized in plants in three enzymatic steps: ligation of glutamate (Glu) to tRNA(Glu) by glutamyl-tRNA synthetase, reduction of activated Glu to Glu-1-semialdehyde by glutamyl-tRNA reductase (GluTR), and transamination to ALA by Glu 1-semialdehyde aminotransferase. ALA formation controls the metabolic flow into the tetrapyrrole biosynthetic pathway. GluTR is proposed to be the key regulatory enzyme that is tightly controlled at transcriptional and posttranslational levels. We identified a GluTR binding protein (GluTRBP; previously called PROTON GRADIENT REGULATION7) that is localized in chloroplasts and part of a 300-kD protein complex in the thylakoid membrane. Although the protein does not modulate activity of ALA synthesis, the knockout of GluTRBP is lethal in Arabidopsis thaliana, whereas mutants expressing reduced levels of GluTRBP contain less heme. GluTRBP expression correlates with a function in heme biosynthesis. It is postulated that GluTRBP contributes to subcompartmentalized ALA biosynthesis by maintaining a portion of GluTR at the plastid membrane that funnels ALA into the heme biosynthetic pathway. These results regarding GluTRBP support a model of plant ALA synthesis that is organized in two separate ALA pools in the chloroplast to provide appropriate substrate amounts for balanced synthesis of heme and chlorophyll.

Keywords

    Agrobacterium tumefaciens/genetics, Aldehyde Oxidoreductases/genetics, Amino Acid Sequence, Aminolevulinic Acid/metabolism, Arabidopsis/genetics, Arabidopsis Proteins/genetics, Carrier Proteins/genetics, Chlorophyll/biosynthesis, Chloroplasts/metabolism, Escherichia coli/genetics, Gene Expression Regulation, Plant, Genes, Plant, Heme/genetics, Molecular Sequence Data, Plants, Genetically Modified/genetics, Plasmids/genetics, Protein Interaction Mapping, RNA Interference, RNA, Plant/genetics, Recombinant Proteins/genetics, Thylakoid Membrane Proteins/genetics, Tobacco/genetics, Transcription, Genetic, Two-Hybrid System Techniques

Cite this

An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. / Czarnecki, Olaf; Hedtke, Boris; Melzer, Michael et al.
In: The plant cell, Vol. 23, No. 12, 12.2011, p. 4476-91.

Research output: Contribution to journalArticleResearchpeer review

Czarnecki, O, Hedtke, B, Melzer, M, Rothbart, M, Richter, A, Schröter, Y, Pfannschmidt, T & Grimm, B 2011, 'An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts', The plant cell, vol. 23, no. 12, pp. 4476-91. https://doi.org/10.1105/tpc.111.086421
Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schröter Y et al. An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. The plant cell. 2011 Dec;23(12):4476-91. doi: 10.1105/tpc.111.086421
Czarnecki, Olaf ; Hedtke, Boris ; Melzer, Michael et al. / An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. In: The plant cell. 2011 ; Vol. 23, No. 12. pp. 4476-91.
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title = "An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts",
abstract = "5-Aminolevulinic acid (ALA) is the universal precursor for tetrapyrrole biosynthesis and is synthesized in plants in three enzymatic steps: ligation of glutamate (Glu) to tRNA(Glu) by glutamyl-tRNA synthetase, reduction of activated Glu to Glu-1-semialdehyde by glutamyl-tRNA reductase (GluTR), and transamination to ALA by Glu 1-semialdehyde aminotransferase. ALA formation controls the metabolic flow into the tetrapyrrole biosynthetic pathway. GluTR is proposed to be the key regulatory enzyme that is tightly controlled at transcriptional and posttranslational levels. We identified a GluTR binding protein (GluTRBP; previously called PROTON GRADIENT REGULATION7) that is localized in chloroplasts and part of a 300-kD protein complex in the thylakoid membrane. Although the protein does not modulate activity of ALA synthesis, the knockout of GluTRBP is lethal in Arabidopsis thaliana, whereas mutants expressing reduced levels of GluTRBP contain less heme. GluTRBP expression correlates with a function in heme biosynthesis. It is postulated that GluTRBP contributes to subcompartmentalized ALA biosynthesis by maintaining a portion of GluTR at the plastid membrane that funnels ALA into the heme biosynthetic pathway. These results regarding GluTRBP support a model of plant ALA synthesis that is organized in two separate ALA pools in the chloroplast to provide appropriate substrate amounts for balanced synthesis of heme and chlorophyll.",
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Download

TY - JOUR

T1 - An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts

AU - Czarnecki, Olaf

AU - Hedtke, Boris

AU - Melzer, Michael

AU - Rothbart, Maxi

AU - Richter, Andreas

AU - Schröter, Yvonne

AU - Pfannschmidt, Thomas

AU - Grimm, Bernhard

PY - 2011/12

Y1 - 2011/12

N2 - 5-Aminolevulinic acid (ALA) is the universal precursor for tetrapyrrole biosynthesis and is synthesized in plants in three enzymatic steps: ligation of glutamate (Glu) to tRNA(Glu) by glutamyl-tRNA synthetase, reduction of activated Glu to Glu-1-semialdehyde by glutamyl-tRNA reductase (GluTR), and transamination to ALA by Glu 1-semialdehyde aminotransferase. ALA formation controls the metabolic flow into the tetrapyrrole biosynthetic pathway. GluTR is proposed to be the key regulatory enzyme that is tightly controlled at transcriptional and posttranslational levels. We identified a GluTR binding protein (GluTRBP; previously called PROTON GRADIENT REGULATION7) that is localized in chloroplasts and part of a 300-kD protein complex in the thylakoid membrane. Although the protein does not modulate activity of ALA synthesis, the knockout of GluTRBP is lethal in Arabidopsis thaliana, whereas mutants expressing reduced levels of GluTRBP contain less heme. GluTRBP expression correlates with a function in heme biosynthesis. It is postulated that GluTRBP contributes to subcompartmentalized ALA biosynthesis by maintaining a portion of GluTR at the plastid membrane that funnels ALA into the heme biosynthetic pathway. These results regarding GluTRBP support a model of plant ALA synthesis that is organized in two separate ALA pools in the chloroplast to provide appropriate substrate amounts for balanced synthesis of heme and chlorophyll.

AB - 5-Aminolevulinic acid (ALA) is the universal precursor for tetrapyrrole biosynthesis and is synthesized in plants in three enzymatic steps: ligation of glutamate (Glu) to tRNA(Glu) by glutamyl-tRNA synthetase, reduction of activated Glu to Glu-1-semialdehyde by glutamyl-tRNA reductase (GluTR), and transamination to ALA by Glu 1-semialdehyde aminotransferase. ALA formation controls the metabolic flow into the tetrapyrrole biosynthetic pathway. GluTR is proposed to be the key regulatory enzyme that is tightly controlled at transcriptional and posttranslational levels. We identified a GluTR binding protein (GluTRBP; previously called PROTON GRADIENT REGULATION7) that is localized in chloroplasts and part of a 300-kD protein complex in the thylakoid membrane. Although the protein does not modulate activity of ALA synthesis, the knockout of GluTRBP is lethal in Arabidopsis thaliana, whereas mutants expressing reduced levels of GluTRBP contain less heme. GluTRBP expression correlates with a function in heme biosynthesis. It is postulated that GluTRBP contributes to subcompartmentalized ALA biosynthesis by maintaining a portion of GluTR at the plastid membrane that funnels ALA into the heme biosynthetic pathway. These results regarding GluTRBP support a model of plant ALA synthesis that is organized in two separate ALA pools in the chloroplast to provide appropriate substrate amounts for balanced synthesis of heme and chlorophyll.

KW - Agrobacterium tumefaciens/genetics

KW - Aldehyde Oxidoreductases/genetics

KW - Amino Acid Sequence

KW - Aminolevulinic Acid/metabolism

KW - Arabidopsis/genetics

KW - Arabidopsis Proteins/genetics

KW - Carrier Proteins/genetics

KW - Chlorophyll/biosynthesis

KW - Chloroplasts/metabolism

KW - Escherichia coli/genetics

KW - Gene Expression Regulation, Plant

KW - Genes, Plant

KW - Heme/genetics

KW - Molecular Sequence Data

KW - Plants, Genetically Modified/genetics

KW - Plasmids/genetics

KW - Protein Interaction Mapping

KW - RNA Interference

KW - RNA, Plant/genetics

KW - Recombinant Proteins/genetics

KW - Thylakoid Membrane Proteins/genetics

KW - Tobacco/genetics

KW - Transcription, Genetic

KW - Two-Hybrid System Techniques

U2 - 10.1105/tpc.111.086421

DO - 10.1105/tpc.111.086421

M3 - Article

C2 - 22180625

VL - 23

SP - 4476

EP - 4491

JO - The plant cell

JF - The plant cell

SN - 1040-4651

IS - 12

ER -

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