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 Edward 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
Pages (from-to)27594-27606
Number of pages13
JournalJournal of Biological Chemistry
Volume288
Issue number38
DOIs
Publication statusPublished - 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 Edward; 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, KE, 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 Edward ; 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.
@article{8f217048ecaa4ee3a248340e4d711515,
title = "Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids",
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.",
author = "Anna Block and Rikard Fristedt and Sara Rogers and Jyothi Kumar and Brian Barnes and Joshua Barnes and Elowsky, {Christian G.} and Yashitola Wamboldt and Mackenzie, {Sally A.} and Redding, {Kevin Edward} and Merchant, {Sabeeha S.} and Basset, {Gilles J.}",
year = "2013",
month = "9",
day = "20",
doi = "10.1074/jbc.M113.492769",
language = "English",
volume = "288",
pages = "27594--27606",
journal = "Journal of Biological Chemistry",
issn = "0021-9258",
publisher = "American Society for Biochemistry and Molecular Biology Inc.",
number = "38",

}

TY - JOUR

T1 - Functional modeling identifies paralogous solanesyl-diphosphate synthases that assemble the side chain of plastoquinone-9 in plastids

AU - Block, Anna

AU - Fristedt, Rikard

AU - Rogers, Sara

AU - Kumar, Jyothi

AU - Barnes, Brian

AU - Barnes, Joshua

AU - Elowsky, Christian G.

AU - Wamboldt, Yashitola

AU - Mackenzie, Sally A.

AU - Redding, Kevin Edward

AU - Merchant, Sabeeha S.

AU - Basset, Gilles J.

PY - 2013/9/20

Y1 - 2013/9/20

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84884563750&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84884563750&partnerID=8YFLogxK

U2 - 10.1074/jbc.M113.492769

DO - 10.1074/jbc.M113.492769

M3 - Article

VL - 288

SP - 27594

EP - 27606

JO - Journal of Biological Chemistry

JF - Journal of Biological Chemistry

SN - 0021-9258

IS - 38

ER -