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Subchromoplast Sequestration of Carotenoids Affects Regulatory Mechanisms in Tomato Lines Expressing Different Carotenoid Gene Combinations

Marilise Nogueira, Leticia Mora, Eugenia M.A. Enfissi, Peter M. Bramley, Paul D. Fraser
Marilise Nogueira
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, United Kingdom
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  • ORCID record for Marilise Nogueira
Leticia Mora
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, United Kingdom
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  • ORCID record for Leticia Mora
Eugenia M.A. Enfissi
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, United Kingdom
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Peter M. Bramley
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, United Kingdom
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Paul D. Fraser
School of Biological Sciences, Royal Holloway University of London, Egham, Surrey TW20 0EX, United Kingdom
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  • ORCID record for Paul D. Fraser
  • For correspondence: p.fraser@rhul.ac.uk

Published November 2013. DOI: https://doi.org/10.1105/tpc.113.116210

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  • © 2013 American Society of Plant Biologists. All rights reserved.

Abstract

Metabolic engineering of the carotenoid pathway in recent years has successfully enhanced the carotenoid contents of crop plants. It is now clear that only increasing biosynthesis is restrictive, as mechanisms to sequestrate these increased levels in the cell or organelle should be exploited. In this study, biosynthetic pathway genes were overexpressed in tomato (Solanum lycopersicum) lines and the effects on carotenoid formation and sequestration revealed. The bacterial Crt carotenogenic genes, independently or in combination, and their zygosity affect the production of carotenoids. Transcription of the pathway genes was perturbed, whereby the tissue specificity of transcripts was altered. Changes in the steady state levels of metabolites in unrelated sectors of metabolism were found. Of particular interest was a concurrent increase of the plastid-localized lipid monogalactodiacylglycerol with carotenoids along with membranous subcellular structures. The carotenoids, proteins, and lipids in the subchromoplast fractions of the transgenic tomato fruit with increased carotenoid content suggest that cellular structures can adapt to facilitate the sequestration of the newly formed products. Moreover, phytoene, the precursor of the pathway, was identified in the plastoglobule, whereas the biosynthetic enzymes were in the membranes. The implications of these findings with respect to novel pathway regulation mechanisms are discussed.

  • Glossary

    CRTI
    phytoene desaturase
    AC
    Ailsa Craig
    MGDG
    monogalactosyldiacylglycerol
    CRTB
    phytoene desaturase
    CRTE
    geranylgeranyl diphosphate synthase
    ACN
    acetonitrile
    MS
    mass spectral
    CAB
    cacodylate buffer
    PB
    phosphate buffer
    LC-MS
    liquid chromatography–mass spectrometry
    nano-LC-MS-MS
    nano–liquid chromatography–tandem mass spectrometry
    • Received July 16, 2013.
    • Revised September 7, 2013.
    • Accepted October 15, 2013.
    • Published November 18, 2013.
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    Subchromoplast Sequestration of Carotenoids Affects Regulatory Mechanisms in Tomato Lines Expressing Different Carotenoid Gene Combinations
    Marilise Nogueira, Leticia Mora, Eugenia M.A. Enfissi, Peter M. Bramley, Paul D. Fraser
    The Plant Cell Nov 2013, 25 (11) 4560-4579; DOI: 10.1105/tpc.113.116210

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    Subchromoplast Sequestration of Carotenoids Affects Regulatory Mechanisms in Tomato Lines Expressing Different Carotenoid Gene Combinations
    Marilise Nogueira, Leticia Mora, Eugenia M.A. Enfissi, Peter M. Bramley, Paul D. Fraser
    The Plant Cell Nov 2013, 25 (11) 4560-4579; DOI: 10.1105/tpc.113.116210
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