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Genetic dissection of cyclic pyranopterin monophosphate biosynthesis in plant mitochondria

Inga Kruse, Andrew Maclean, Lionel Hill, Janneke Balk
doi: https://doi.org/10.1101/234450
Inga Kruse
1John Innes Centre, Norwich NR4 7UH, UK
2University of East Anglia, Norwich NR4 7TJ, UK
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Andrew Maclean
1John Innes Centre, Norwich NR4 7UH, UK
2University of East Anglia, Norwich NR4 7TJ, UK
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Lionel Hill
1John Innes Centre, Norwich NR4 7UH, UK
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Janneke Balk
1John Innes Centre, Norwich NR4 7UH, UK
2University of East Anglia, Norwich NR4 7TJ, UK
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Abstract

Mitochondria play a key role in the biosynthesis of two metal cofactors, iron-sulfur (FeS) clusters and molybdenum cofactor (Moco). The two pathways intersect at several points, but a scarcity of mutants has hindered studies to better understand these links. We screened a collection of sirtinol-resistant Arabidopsis thaliana mutants for lines with decreased activities of cytosolic FeS enzymes and Moco enzymes. We identified a new mutant allele of ATM3, encoding the ATP-binding cassette Transporter of the Mitochondria 3 (systematic name ABCB25), confirming the previously reported role of ATM3 in both FeS cluster and Moco biosynthesis. We also identified a mutant allele in CNX2, Cofactor of Nitrate reductase and Xanthine dehydrogenase 2, encoding GTP 3′,8-cyclase, the first step in Moco biosynthesis which is localized in the mitochondria. A single nucleotide polymorphism in cnx2-2 leads to substitution of Arg88 with Gln in the N-terminal FeS cluster-binding motif. cnx2-2 plants are small and chlorotic, with severely decreased Moco enzyme activities, but they performed better than a cnx2-1 knockout mutant, which could only survive with ammonia as nitrogen source. Measurement of cyclic pyranopterin monophosphate (cPMP) levels by LC-MS/MS showed that this Moco intermediate was below the limit of detection in both cnx2-1 and cnx2-2, and accumulated more than 10-fold in seedlings mutated in the downstream gene CNX5. Interestingly, atm3-1 mutants had less cPMP than wild type, correlating with previous reports of a similar decrease in nitrate reductase activity. Taken together, our data functionally characterise CNX2 and suggest that ATM3 is indirectly required for cPMP synthesis.

  • Abbreviations

    ABA3
    abscisic acid protein 3
    ABC
    ATP-binding cassette
    ATM3
    ABC transporter of the mitochondria 3
    AldOx
    aldehyde oxidase
    cPMP
    cyclic pyranopterin monophosphate
    CNX
    cofactor of nitrate reductase and xanthine dehydrogenase
    Col-0
    Columbia-0 ecotype
    EMS
    ethyl methanesulfonate
    F1
    filial 1
    FeS
    iron-sulfur
    GSSG
    glutathione disulfide
    GS-S-SG
    glutathione trisulfide
    ISU/ISCU
    iron-sulfur cluster assembly protein 1
    Ler
    Landsberg ecotype
    mARC
    mitochondrial amidoxime-reducing component
    Moco
    molybdenum cofactor
    MOCS
    molybdenum cofactor synthesis protein
    NFS1
    nitrogen fixation S (NIFS)-like 1
    SAM
    S-adenosylmethionine
    SNP
    single nucleotide polymorphism
    SSLP
    simple sequence length polymorphism
    T-DNA
    transfer DNA
    TMH
    transmembrane helix
    TOM40
    translocator of the outer membrane 40
    URM
    ubiquitin-related modifier
    XDH
    xanthine dehydrogenase
  • Copyright 
    The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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    Posted December 14, 2017.
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    Genetic dissection of cyclic pyranopterin monophosphate biosynthesis in plant mitochondria
    Inga Kruse, Andrew Maclean, Lionel Hill, Janneke Balk
    bioRxiv 234450; doi: https://doi.org/10.1101/234450
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    Genetic dissection of cyclic pyranopterin monophosphate biosynthesis in plant mitochondria
    Inga Kruse, Andrew Maclean, Lionel Hill, Janneke Balk
    bioRxiv 234450; doi: https://doi.org/10.1101/234450

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