Disruption of a horizontally transferred phytoene desaturase abolishes carotenoid accumulation and diapause in Tetranychus urticae

  1. Bryon, A. 6
  2. Kurlovs, A.H. 1
  3. Dermauw, W. 6
  4. Greenhalgh, R. 1
  5. Riga, M. 48
  6. Grbic, M. 25
  7. Tirry, L. 6
  8. Osakabe, M. 7
  9. Vontas, J. 89
  10. Clark, R.M. 11
  11. Leeuwen, T.V. 36
  1. 1 University of Utah
    info

    University of Utah

    Salt Lake City, Estados Unidos

    ROR https://ror.org/03r0ha626

  2. 2 University of Western Ontario
    info

    University of Western Ontario

    London, Canadá

    ROR https://ror.org/02grkyz14

  3. 3 University of Amsterdam
    info

    University of Amsterdam

    Ámsterdam, Holanda

    ROR https://ror.org/04dkp9463

  4. 4 Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology Hellas, Heraklion, Crete, Greece
  5. 5 Instituto de Ciencias de la Vid y del Vino
    info

    Instituto de Ciencias de la Vid y del Vino

    Logroño, España

    ROR https://ror.org/01rm2sw78

  6. 6 Ghent University
    info

    Ghent University

    Gante, Bélgica

    ROR https://ror.org/00cv9y106

  7. 7 Kyoto University
    info

    Kyoto University

    Kioto, Japón

    ROR https://ror.org/02kpeqv85

  8. 8 University of Crete
    info

    University of Crete

    Heraklion, Grecia

    ROR https://ror.org/00dr28g20

  9. 9 Agricultural University of Athens
    info

    Agricultural University of Athens

    Atenas, Grecia

    ROR https://ror.org/03xawq568

Revista:
Proceedings of the National Academy of Sciences of the United States of America

ISSN: 0027-8424

Año de publicación: 2017

Volumen: 114

Número: 29

Páginas: E5871-E5880

Tipo: Artículo

DOI: 10.1073/PNAS.1706865114 SCOPUS: 2-s2.0-85025094466 WoS: WOS:000405662300016 GOOGLE SCHOLAR

Otras publicaciones en: Proceedings of the National Academy of Sciences of the United States of America

Repositorio institucional: lock_openAcceso abierto Editor

Resumen

Carotenoids underlie many of the vibrant yellow, orange, and red colors in animals, and are involved in processes ranging from vision to protection from stresses. Most animals acquire carotenoids from their diets because de novo synthesis of carotenoids is primarily limited to plants and some bacteria and fungi. Recently, sequencing projects in aphids and adelgids, spider mites, and gall midges identified genes with homology to fungal sequences encoding de novo carotenoid biosynthetic proteins like phytoene desaturase. The finding of horizontal gene transfers of carotenoid biosynthetic genes to three arthropod lineages was unprecedented; however, the relevance of the transfers for the arthropods that acquired them has remained largely speculative, which is especially true for spider mites that feed on plant cell contents, a known source of carotenoids. Pigmentation in spider mites results solely from carotenoids. Using a combination of genetic approaches, we show that mutations in a single horizontally transferred phytoene desaturase result in complete albinism in the twospotted spider mite, Tetranychus urticae, as well as in the citrus red mite, Panonychus citri. Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of T. urticae, consistent with a role for this enzyme in provisioning provitamin A carotenoids required for light perception. Carotenoid biosynthetic genes of fungal origin have therefore enabled some mites to forgo dietary carotenoids, with endogenous synthesis underlying their intense pigmentation and ability to enter diapause, a key to the global distribution of major spider mite pests of agriculture.