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

Astrid Bryon, Andre H. Kurlovs, Wannes Dermauw, Robert Greenhalgh, Maria Riga, Miodrag Grbic, Luc Tirry, Masahiro Osakabe, John Vontas, Richard M. Clark, Thomas Van Leeuwen*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

30 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)E5871-E5880
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number29
DOIs
Publication statusPublished - 18 Jul 2017
Externally publishedYes

Keywords

  • Bulked segregant analysis
  • Horizontal gene transfer
  • Spider mites
  • Xanthophylls
  • β-carotene

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