Shared Transcriptional Control and Disparate Gain and Loss of Aphid Parasitism Genes

Abstract

Aphids are a diverse group of taxa that contain agronomically important species, which vary in their host range and ability to infest crop plants. The genome evolution underlying agriculturally important aphid traits is not well understood. We generated draft genome assemblies for two aphid species: Myzus cerasi (black cherry aphid) and the cereal specialist Rhopalosiphum padi. Using a de novo gene prediction pipeline on both these, and three additional aphid genome assemblies (Acyrthosiphon pisum, Diuraphis noxia, and Myzus persicae), we show that aphid genomes consistently encode similar gene numbers. We compare gene content, gene duplication, synteny, 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. Putative effector repertoires, originating from duplicated and other loci, have an unusual genomic organization and evolutionary history. We identify a highly conserved effector pair that is tightly physically linked in the genomes of all aphid species tested. In R. padi, this effector pair is tightly transcriptionally linked and shares an unknown transcriptional control mechanism with a subset of ∼50 other putative effectors and secretory proteins. This study extends our current knowledge on the evolution of aphid genomes and reveals evidence for an as-of-yet unknown shared control mechanism, which underlies effector expression, and ultimately plant parasitism.

Improved genome assembly and annotation of the soybean aphid (Aphis glycinesMatsumura)

“…I assessed gene-level completeness of A. glycines v1 (A_gly_v1) and other published aphid genome assemblies using Benchmarking Universal Single-Copy Orthologs (BUSCO) v3.0 (Waterhouse et al 2018;Simão et al 2015) with the Arthropoda gene set (n = 1,066) using default settings. I obtained the publicly available genome assemblies of A. glycines v1 (A_gly_v1) (Wenger et al 2017), Acyrthosiphon pisum (LSR1) v2.1b (IAGC 2010), Diuraphis noxia (Nicholson et al 2015), Myzus cerasi (Thorpe et al 2018), Myzus persicae (G006) v1.1 (Mathers et al 2017) and Rhopalosiphum padi (Thorpe et al 2018) from AphidBase (bipaa.genouest.org/is/aphidbase/). I also included the recently published high quality assembly of Rhopalosiphum maidis ).…”

“…They are also important models used to study plant-insect interactions (Hogenhout and Bos 2011;Ferry et al 2004), speciation genomics (Pecoud and Simon 2010;Peccoud et al 2009;Hawthorne and Via 2001) and sex chromosome evolution (Jaquiéry et al 2018(Jaquiéry et al , 2013. Despite their importance, only a small number of the approximately 5,000 described aphid species have had their genomes sequenced (IAGC 2010;Nicholson et al 2015;Wenger et al 2017;Mathers et al 2017;Chen et al 2019;Jiang et al 2019;Quan et al 2019; Thorpe et al 2018), limiting genomic insights into their diversity and evolution. Furthermore, although highly contiguous assemblies have recently been published for two aphid species (Jiang et al 2019;Chen et al 2019), the majority of publicly available aphid genomes were sequenced using second-generation short-read sequencing technology, resulting in fragmented assemblies that contain thousands of genomic scaffolds.…”

An aphid effector promotes barley susceptibility through suppression of defence gene expression

“…Effector sequence divergence between the aphid species R. padi and M. persicae 95 We predicted putative orthologs for 3 previously described M. persicae effectors, MpC002, 96 Mp1 and Mp58 from R. padi using reciprocal best blast hit analyses on available aphid 97 transcriptome datasets and aphid genome assemblies (threshold of 70 % identity and 98 50 % query coverage) (Thorpe et al, 2016;Thorpe et al, 2018). To confirm the sequences 99 of putative orthologous effector pairs we cloned and sequenced their coding sequences.…”

Population genetic structure and predominance of cyclical parthenogenesis in the bird cherry‐oat aphid Rhopalosiphum padi in England

“…Gene prediction was done with Augustus v3.3.1 (Stanke, Diekhans, Baertsch, & Haussler, 2008) using the same trained set of genes used by Thorpe et al (2018) and RNAseq exon and intron hints.…”

“…3,625; Figure S1). These long reads were used together with the short Illumina reads generated by Thorpe et al (2018) to assemble a new genome using MaSuRCA. The resulting assembly has a length of 321,589,008 bp, which is similar to the length of the previous genome version (…”