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

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 two-spotted spider mite, , as well as in the citrus red mite, Further, we show that phytoene desaturase activity is essential for photoperiodic induction of diapause in an overwintering strain of , 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.

Kin competition accelerates experimental range expansion in an arthropod herbivore

“…The strain ALBINO was resequenced in the context of a genetic mapping study (Bryon et al . ), confirming genome‐wide homozygosity and providing proof‐of‐principle of the methods applied (see Appendix S5). Inbred lines do not show indications of genetic load for traits related to reproduction and survival (see Appendix S2).…”

Environmental RNA interference in two-spotted spider mite,Tetranychus urticae, reveals dsRNA processing requirements for efficient RNAi response

“…Furthermore, the candidate loci underlying mite physiological processes (e.g. diapause, carotene biosynthesis) and pesticide resistance using forward genetic approaches have been recently identified 25,26 . However, the assessment of the in vivo function of candidate loci, at the level of otherwise unperturbed whole organism, is so far lacking.…”

Genomes of trombidid mites reveal novel predicted allergens and laterally-transferred genes associated with secondary metabolism

“…While colouration is not known to be factor during courtship, the males of some species deposit spermatophores in specially constructed “gardens” and perform encircling dances with the female [18]. However, it has recently been discovered using genetic manipulation of a laterally-transferred phytoene desaturase that carotenoids have a second, distinct function in the regulation of diapause in T. urticae [13]. A lack of phytoene desaturase activity not only results in albinism, but prevents overwintering strains from entering diapause, probably due to disrupted light (and thus photoperiod) perception caused by vitamin A deficiency.…”

“…One group of acariform mites, the spider mites (superfamily Tetranychoidea: order Trombidiformes; Fig. 1), are major pests of various crops and rely on well-characterised lateral gene transfers of β-cyanoalanine synthase (from bacteria) and carotenoid biosynthesis enzymes (from fungi) to detoxify hydrogen cyanide in their diet [12] and to control diapause [13], respectively. Currently, it is unknown whether LGT is a key feature of the evolution of the spider mites only, or is more widespread among the Trombidiformes.…”