Phylloxerids share ancestral carotenoid biosynthesis genes of fungal origin with aphids and adelgids.

Chaoyang Zhao,Paul D Nabity,Daniel Doucet

doi:10.1371/journal.pone.0185484

Chaoyang Zhao, Paul D Nabity + Show 1 more

Open Access

https://doi.org/10.1371/journal.pone.0185484

Copy DOI

Journal: PloS one	Publication Date: Oct 11, 2017
Citations: 21	License type: CC BY 4.0

Affiliation: University of California, Riverside

Abstract

Gene transfer among reproductively isolated organisms can lead to novel phenotypes and increased fitness. Among the Sternorrhyncha, a suborder of plant sap-feeding hemipteran insects, both aphids and adelgids acquired carotenoid biosynthesis genes from a fungal donor that result in ecologically relevant pigmentation. Phylloxerids form another family that are closely related to aphids and adelgids and share similar pigmentation, but are largely uncharacterized for their presence and number of pigment genes that have duplicated among aphids. Here, we examined the transcriptomes of nine phylloxerid species, and performed PCR to amplify carotenoid genes from their genomic DNA. We identified carotenoid cyclase/synthase and desaturase genes in each species and demonstrated that they share the common fungal origin as those of aphids and adelgids based on their exon-intron gene structures and phylogenetic relationships. The phylogenetic analyses also indicated that carotenoid genes evolved following the differentiation of aphids, adelgids, and phylloxerids at the levels of family, genus, and species. Unlike aphids that duplicated these genes in their genomes, phylloxerids maintained only single copies, and some species may lack expression of certain genes. These results suggest that the phylloxerid lifestyle undergoes reduced selection pressure to expand carotenoid synthesis genes, and provides insight into these gene functions in insects.

Highlights

In contrast with traditional reproduction where genes are transmitted vertically from a parent to offspring, horizontal or lateral gene transfer (HGT or LGT) is the transmission of genes between reproductively isolated organisms
We identified the cartotenoid cyclase/synthase and desaturase genes in nine Phylloxeridae species from their RNAseq assemblies and/or using a genomic DNA PCR approach
NCBI Non-redundant protein database with the top BLASTP hit Ac. pisum XP_003241670 (NCBI accession #). These Phylloxeridae carotenoid genes were horizontally acquired, they seem to be derived from a single HGT event through which single copies of cyclase/synthase and desaturase were incorporated into the genome of the common ancestor from a fungus, possibly an endosymbiont of the ancestor

Summary

Introduction

In contrast with traditional reproduction where genes are transmitted vertically from a parent to offspring, horizontal or lateral gene transfer (HGT or LGT) is the transmission of genes between reproductively isolated organisms. A great number of reported HGT events occur between microorganisms, recent studies demonstrate that insects readily incorporate foreign genes into their genomes [2]. Next-generation sequencing technologies have facilitated the discovery of microbial genes incorporated into the genomes of insect species belonging to a variety of orders including. Some horizontally acquired genes undergo degradation through mutational processes such as frame-shift gene mutations and eventually become pseudogenes, many genes remain and evolve functional roles that increase the fitness of recipient organisms. Several studies indicated that the acquisition of microbial genes in insect genomes facilitates nutrient digestion and metabolism, including the catabolism of dietary carbohydrates and the biosynthesis of amino acids, vitamins, and carotenoids [2, 13,14,15,16,17,18,19]

Methods

Results

Conclusion