Carotenoids are colored compounds produced by plants, fungi, and microorganisms. Pea aphids can appear in a red or green color, and the carotenoid torulene occurs only in red pea aphids. The aphid genome encodes multiple enzymes for carotenoid biosynthesis. These genes are derived from fungal genes, which have been integrated into the aphid genome and duplicated. A mutation of a certain region in the red aphid genome that encodes a single carotenoid desaturase results in a loss of forulene and red body color, meaning that aphids make their own carotenoids.
Green pea aphids contain alpha, beta and gamma carotene, and red pea aphids contain all of these plus torulene. There are three hypotheses that researchers have for the presence of carotenoids in aphids. The first is that they were obtained from aphid diets, but because carotenoids are not expected to exist significantly in phloem sap, and because carotenoid profiles of aphids and host plants are very different, this hypothesis is not the case. The second hypothesis is that aphids acquired carotenoids through bacterial endosymbiosis, but because aphid carotenoid biosynthetic genes are not homologous to primary symbionts, this hypothesis is not the case either. The third hypothesis is that aphids make their own carotenoids through genes that were laterally transferred from fungi.
Figures and Results
A GenBank protein database search was carried out and revealed that the closest sequence homology to pea aphid biosynthetic genes was found in several fungi and no other animal. Phylogenetic analyses revealed that aphid copies of carotenoid desaturase proteins and carotenoid cyclase-carotenoid synthase proteins form a clade that is nested within a fungal clade. Figure 2 clearly shows that aphid carotenoid biosynthesis genes indeed form a distinct clade that is nested within those of fungi. They also show a single origin of these genes within fungi. Furthermore, the gene arrangement between pea aphids and certain fungi were found to be similar. A point mutation was induced on a red aphid carotenoid desaturase coding region, and it resulted in the inability of these aphids to make toluene.
The aforementioned evidence reveals that aphid carotenoid genes were transferred from a fungus to an aphid ancestor as a single event and that subsequent gene duplication occurred. The transfer preserved the gene arrangement observed in fungi. The red-green polymorphism observed in pea aphids because of the lack or presence of torulene results in differential susceptibility by natural predators. This is to say that, depending on the visual cues that different predators use to find prey, it may be more advantageous for aphids to appear as one color over the other, increasing the frequency of the phenotype.