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Differential regulation of the Tor gene homolog drives the red/green pigmentation phenotype in the aphid Myzus persicae.

Trissi, N, Troczka, BJ, Ozsanlav-Harris, L, Singh, KS, Mallott, M, Aishwarya, V, O'Reilly, A, Bass, C and Wilding, CS (2023) Differential regulation of the Tor gene homolog drives the red/green pigmentation phenotype in the aphid Myzus persicae. Insect Biochemistry and Molecular Biology, 153. ISSN 0965-1748

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Open Access URL: https://doi.org/10.1016/j.ibmb.2022.103896 (Published version)

Abstract

In some aphid species, intraspecific variation in body colour is caused by differential carotenoid content: whilst green aphids contain only yellow carotenoids (β-, γ-, and β,γ-carotenes), red aphids additionally possess red carotenoids (torulene and 3,4-didehydrolycopene). Unusually, within animals who typically obtain carotenoids from their diet, ancestral horizontal gene transfer of carotenoid biosynthetic genes from fungi (followed by gene duplication), have imbued aphids with the intrinsic gene repertoire necessary to biosynthesise carotenoids. In the pea aphid, Acyrthosiphon pisum a lycopene (phytoene) desaturase gene (Tor) underpins the red/green phenotype, with this locus present in heterozygous form in red individuals but absent in green aphids, resulting in them being unable to convert lycopene into the red compounds 3,4-didehydrolycopene and torulene. The green peach aphid, Myzus persicae, separated from the pea aphid for ≈45MY also exists as distinct colour variable morphs, with both red and green individuals present. Here, we examined genomic data for both red and green morphs of M. persicae and identified an enlarged (compared to A. pisum) repertoire of 16 carotenoid biosynthetic genes (11 carotenoid desaturases and five carotenoid cyclase/synthase genes). From these, we identify the homolog of A. pisum Tor (here called carotene desaturase 2 or CDE-2) and show through 3D modelling that this homolog can accommodate the torulene precursor lycopene and, through RNA knockdown feeding experiments, demonstrate that disabling CDE-2 expression in red M. persicae clones results in green-coloured offspring. Unlike in A. pisum, we show that functional CDE-2 is present in the genomes of both red and green aphids. However, expression differences between the two colour morphs (350-700 fold CDE-2 overexpression in red clones), potentially driven by variants identified in upstream putative regulatory elements, underpin this phenotype. Thus, whilst aphids have a common origin of their carotenoid biosynthetic pathway, two aphid species separated for over 40MY have evolved very different drivers of intraspecific colour variation.

Item Type: Article
Uncontrolled Keywords: Aphid; Carotene; Carotenoid; Colour polymorphism; Gene expression; 0304 Medicinal and Biomolecular Chemistry; 0601 Biochemistry and Cell Biology; 0608 Zoology; Entomology
Subjects: Q Science > QH Natural history > QH301 Biology
Q Science > QH Natural history > QH426 Genetics
Q Science > QL Zoology
Divisions: Biological & Environmental Sciences (from Sep 19)
Publisher: Elsevier
SWORD Depositor: A Symplectic
Date Deposited: 06 Jan 2023 10:37
Last Modified: 06 Jan 2023 10:45
DOI or ID number: 10.1016/j.ibmb.2022.103896
URI: https://researchonline.ljmu.ac.uk/id/eprint/18545
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