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Shared transcriptional control and disparate gain and loss of aphid parasitism genes and loci acquired via horizontal gene transfer

By Peter Thorpe, Carmen M. Escudero-Martinez, Peter J. A. Cock, D. Laetsch, Sebastian Eves-van den Akker, Jorunn IB Bos

Posted 11 Jan 2018
bioRxiv DOI: 10.1101/246801

Background: Aphids are a diverse group of taxa that contain hundreds of agronomically important species, which vary in their host range and pathogenicity. However, the genome evolution underlying agriculturally important aphid traits is not well understood. Results: We generated highly-contiguous draft genome assemblies for two aphid species: the narrow host range Myzus cerasi, and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these genome assemblies, and those of three related species (Acyrthosiphon pisum, D. noxia and M. persicae), we show that aphid genomes consistently encode similar gene numbers, and in the case of A. pisum, fewer and larger genes than previously reported. We compare gene content, gene duplication, synteny, horizontal gene transfer events, and putative effector repertoires between these five species to understand the genome evolution of globally important plant parasites. Aphid genomes show signs of relatively distant gene duplication, and substantial, relatively recent, gene birth, and are characterized by disparate gain and loss of genes acquired by horizontal gene transfer (HGT). Such HGT events account for approximately 1% of loci, and contribute to the protein-coding content of aphid species analysed. Putative effector repertoires, originating from duplicated loci, putative HGT events and other loci, have an unusual genomic organisation and evolutionary history. We identify a highly conserved effector-pair that is tightly genetically-linked in all aphid species. In R. padi, this effector pair is tightly transcriptionally-linked, and shares a transcriptional control mechanism with a subset of approximately 50 other putative effectors distributed across the genome. Conclusions: This study extends our current knowledge on the evolution of aphid genomes and reveals evidence for a shared control mechanism, which underlies effector expression, and ultimately plant parasitism. Note: Sebastian Eves-van den Akker and Jorunn Bos are co-corresponding authors.

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