SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato

Authors

  • Jonathan T. Vogel,

    1. Horticultural Sciences Department and the Plant Molecular & Cellular Biology Program, University of Florida, Gainesville, Florida 32611, USA
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    • Present address: BASF Plant Science, 26 Davis Drive, Research Triangle Park, NC 27709 USA.

  • Michael H. Walter,

    1. Leibniz-Institut für Pflanzenbiochemie, Abteilung Sekundärstoffwechsel, D–06120 Halle (Saale), Germany
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  • Patrick Giavalisco,

    1. Max Planck Institute of Molecular Plant Physiology, D–14476 Potsdam-Golm, Germany
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  • Anna Lytovchenko,

    1. Max Planck Institute of Molecular Plant Physiology, D–14476 Potsdam-Golm, Germany
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  • Wouter Kohlen,

    1. Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
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  • Tatsiana Charnikhova,

    1. Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
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  • Andrew J. Simkin,

    1. Horticultural Sciences Department and the Plant Molecular & Cellular Biology Program, University of Florida, Gainesville, Florida 32611, USA
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    • Present address: Biomolécule et Biotechnologie Végétale, EA2106, Université François-Rabelais Tours, 37200 France.

  • Charles Goulet,

    1. Horticultural Sciences Department and the Plant Molecular & Cellular Biology Program, University of Florida, Gainesville, Florida 32611, USA
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  • Dieter Strack,

    1. Leibniz-Institut für Pflanzenbiochemie, Abteilung Sekundärstoffwechsel, D–06120 Halle (Saale), Germany
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  • Harro J. Bouwmeester,

    1. Laboratory of Plant Physiology, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
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  • Alisdair R. Fernie,

    1. Max Planck Institute of Molecular Plant Physiology, D–14476 Potsdam-Golm, Germany
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  • Harry J. Klee

    Corresponding author
    1. Horticultural Sciences Department and the Plant Molecular & Cellular Biology Program, University of Florida, Gainesville, Florida 32611, USA
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For correspondence (fax (352) 846 2063; e-mail hjklee@ufl.edu).

Summary

The regulation of shoot branching is an essential determinant of plant architecture, integrating multiple external and internal signals. One of the signaling pathways regulating branching involves the MAX (more axillary branches) genes. Two of the genes within this pathway, MAX3/CCD7 and MAX4/CCD8, encode carotenoid cleavage enzymes involved in generating a branch-inhibiting hormone, recently identified as strigolactone. Here, we report the cloning of SlCCD7 from tomato. As in other species, SlCCD7 encodes an enzyme capable of cleaving cyclic and acyclic carotenoids. However, the SlCCD7 protein has 30 additional amino acids of unknown function at its C terminus. Tomato plants expressing a SlCCD7 antisense construct display greatly increased branching. To reveal the underlying changes of this strong physiological phenotype, a metabolomic screen was conducted. With the exception of a reduction of stem amino acid content in the transgenic lines, no major changes were observed. In contrast, targeted analysis of the same plants revealed significantly decreased levels of strigolactone. There were no significant changes in root carotenoids, indicating that relatively little substrate is required to produce the bioactive strigolactones. The germination rate of Orobanche ramosa seeds was reduced by up to 90% on application of extract from the SlCCD7 antisense lines, compared with the wild type. Additionally, upon mycorrhizal colonization, C13 cyclohexenone and C14 mycorradicin apocarotenoid levels were greatly reduced in the roots of the antisense lines, implicating SlCCD7 in their biosynthesis. This work demonstrates the diverse roles of MAX3/CCD7 in strigolactone production, shoot branching, source–sink interactions and production of arbuscular mycorrhiza-induced apocarotenoids.

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