Convergent evolution of cytochrome P450s underlies independent origins of keto-carotenoid pigmentation in animals

Nicky Wybouw, Andre H. Kurlovs, Robert Greenhalgh, Astrid Bryon, Olivia Kosterlitz, Yuki Manabe, Masahiro Osakabe, John Vontas, Richard M. Clark*, Thomas Van Leeuwen

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

Abstract

Keto-carotenoids contribute to many important traits in animals, including vision and coloration. In a great number of animal species, keto-carotenoids are endogenously produced from carotenoids by carotenoid ketolases. Despite the ubiquity and functional importance of keto-carotenoids in animals, the underlying genetic architectures of their production have remained enigmatic. The body and eye colorations of spider mites (Arthropoda: Chelicerata) are determined by b-carotene and keto-carotenoid derivatives. Here, we focus on a carotenoid pigment mutant of the spider mite Tetranychus kanzawai that, as shown by chromatography, lost the ability to produce keto-carotenoids. We employed bulked segregant analysis and linked the causal locus to a single narrow genomic interval. The causal mutation was fine-mapped to a minimal candidate region that held only one complete gene, the cytochrome P450 monooxygenase CYP384A1, of the CYP3 clan. Using a number of genomic approaches, we revealed that an inactivating deletion in the fourth exon of CYP384A1 caused the aberrant pigmentation. Phylogenetic analysis indicated that CYP384A1 is orthologous across mite species of the ancient Trombidiformes order where carotenoids typify eye and body coloration, suggesting a deeply conserved function of CYP384A1 as a carotenoid ketolase. Previously, CYP2J19, a cytochrome P450 of the CYP2 clan, has been identified as a carotenoid ketolase in birds and turtles. Our study shows that selection for endogenous production of keto-carotenoids led to convergent evolution, whereby cytochrome P450s were independently co-opted in vertebrate and invertebrate animal lineages.

Original languageEnglish
Article number20191039
JournalProceedings of the Royal Society B: Biological Sciences
Volume286
Issue number1907
DOIs
Publication statusPublished - 24 Jul 2019
Externally publishedYes

Keywords

  • Carotenoid ketolase
  • Convergent evolution
  • CYP384A1
  • Keto-carotenoids
  • Lemon

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