Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids

Anna Block, Rikard Fristedt, Sara Rogers, Jyothi Kumar, Brian Barnes, Joshua Barnes, Christian G. Elowsky, Yashitola Wamboldt, Sally A. Mackenzie, Kevin Redding, Sabeeha S. Merchant, Gilles J. Basset

    Research output: Contribution to journalArticle

    25 Citations (Scopus)

    Abstract

    It is a little known fact that plastoquinone-9, a vital redox cofactor of photosynthesis, doubles as a precursor for the biosynthesis of a vitamin E analog called plastochromanol-8, the physiological significance of which has remained elusive. Gene network reconstruction, GFP fusion experiments, and targeted metabolite profiling of insertion mutants indicated that Arabidopsis possesses two paralogous solanesyl-diphosphate synthases, AtSPS1 (At1g78510) and AtSPS2 (At1g17050), that assemble the side chain of plastoquinone-9 in plastids. Similar paralogous pairs were detected throughout terrestrial plant lineages but were not distinguished in the literature and genomic databases from mitochondrial homologs involvedin the biosynthesis of ubiquinone. The leaves of the atsps2 knock-out were devoidofplastochromanol-8 and displayed severe lossesofboth non-photoactive and photoactive plastoquinone-9, resulting in near complete photoinhibition at high light intensity. Such a photoinhibition was paralleled by significant damage to photosystem II but not to photosystem I. In contrast, in the atsps1 knock-out, a small loss of plastoquinone-9, restricted to the non-photoactive pool, was sufficient to eliminate half of the plastochromanol-8 content of the leaves. Taken together, these results demonstrate that plastochromanol-8 originates from a subfraction of the non-photoactive pool of plastoquinone-9. In contrast to other plastochromanol-8 biosynthetic mutants, neither the single atsps knock-outs nor the atsps1 atsps2 double knock-out displayed any defectsintocopherols accumulation or germination.

    Original languageEnglish (US)
    Pages (from-to)27594-27606
    Number of pages13
    JournalJournal of Biological Chemistry
    Volume288
    Issue number38
    DOIs
    StatePublished - Sep 20 2013

    Fingerprint

    Plastoquinone
    Plastids
    Biosynthesis
    High intensity light
    Photosystem I Protein Complex
    Ubiquinone
    Photosystem II Protein Complex
    Photosynthesis
    Gene Regulatory Networks
    Germination
    Metabolites
    Vitamin E
    Arabidopsis
    Oxidation-Reduction
    Fusion reactions
    Genes
    trans-octaprenyltranstransferase
    Databases
    Light
    plastochromanol 8

    ASJC Scopus subject areas

    • Biochemistry
    • Cell Biology
    • Molecular Biology

    Cite this

    Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids. / Block, Anna; Fristedt, Rikard; Rogers, Sara; Kumar, Jyothi; Barnes, Brian; Barnes, Joshua; Elowsky, Christian G.; Wamboldt, Yashitola; Mackenzie, Sally A.; Redding, Kevin; Merchant, Sabeeha S.; Basset, Gilles J.

    In: Journal of Biological Chemistry, Vol. 288, No. 38, 20.09.2013, p. 27594-27606.

    Research output: Contribution to journalArticle

    Block, A, Fristedt, R, Rogers, S, Kumar, J, Barnes, B, Barnes, J, Elowsky, CG, Wamboldt, Y, Mackenzie, SA, Redding, K, Merchant, SS & Basset, GJ 2013, 'Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids' Journal of Biological Chemistry, vol. 288, no. 38, pp. 27594-27606. https://doi.org/10.1074/jbc.M113.492769
    Block, Anna ; Fristedt, Rikard ; Rogers, Sara ; Kumar, Jyothi ; Barnes, Brian ; Barnes, Joshua ; Elowsky, Christian G. ; Wamboldt, Yashitola ; Mackenzie, Sally A. ; Redding, Kevin ; Merchant, Sabeeha S. ; Basset, Gilles J. / Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids. In: Journal of Biological Chemistry. 2013 ; Vol. 288, No. 38. pp. 27594-27606.
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    abstract = "It is a little known fact that plastoquinone-9, a vital redox cofactor of photosynthesis, doubles as a precursor for the biosynthesis of a vitamin E analog called plastochromanol-8, the physiological significance of which has remained elusive. Gene network reconstruction, GFP fusion experiments, and targeted metabolite profiling of insertion mutants indicated that Arabidopsis possesses two paralogous solanesyl-diphosphate synthases, AtSPS1 (At1g78510) and AtSPS2 (At1g17050), that assemble the side chain of plastoquinone-9 in plastids. Similar paralogous pairs were detected throughout terrestrial plant lineages but were not distinguished in the literature and genomic databases from mitochondrial homologs involvedin the biosynthesis of ubiquinone. The leaves of the atsps2 knock-out were devoidofplastochromanol-8 and displayed severe lossesofboth non-photoactive and photoactive plastoquinone-9, resulting in near complete photoinhibition at high light intensity. Such a photoinhibition was paralleled by significant damage to photosystem II but not to photosystem I. In contrast, in the atsps1 knock-out, a small loss of plastoquinone-9, restricted to the non-photoactive pool, was sufficient to eliminate half of the plastochromanol-8 content of the leaves. Taken together, these results demonstrate that plastochromanol-8 originates from a subfraction of the non-photoactive pool of plastoquinone-9. In contrast to other plastochromanol-8 biosynthetic mutants, neither the single atsps knock-outs nor the atsps1 atsps2 double knock-out displayed any defectsintocopherols accumulation or germination.",
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    AU - Barnes, Joshua

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