Chromosome-scale genome assemblies of aphids reveal extensively rearranged autosomes and long-term conservation of the X chromosome

Abstract

Large-scale chromosome rearrangements are arguably the most dramatic type of mutations, often leading to rapid evolution and speciation. However, chromosome dynamics have only been studied at the sequence level in a small number of model systems. In insects, Diptera (flies and mosquitoes) and Lepidoptera (butterflies and moths) have high levels of chromosome conservation. Whether this truly reflects the diversity of insect genome evolution is questionable given that many species exhibit rapid karyotype evolution. Here, we investigate chromosome evolution in aphids -an important group of hemipteran plant pests -using newly generated chromosome-scale genome assemblies of the green peach aphid (Myzus persicae) and the pea aphid (Acyrthosiphon pisum), and a previously published chromosome-scale assembly of the corn-leaf aphid (Rhopalosiphum maidis). We find that aphid autosomes have undergone dramatic reorganisation over the last 30 million years, to the extent that chromosome homology cannot be determined between aphids from the tribes Macrosiphini (M. persicae and A. pisum) and Aphidini (R. maidis). In contrast, gene content of the aphid sex (X) chromosome remained unchanged despite rapid sequence evolution, low gene expression and high transposable element load. To test whether rapid evolution of genome structure is a hallmark of Hemiptera, we compared our aphid assemblies to chromosome-level assemblies of two blood-feeding Hemiptera (Rhodnius prolixus and Triatoma rubrofasciata). Despite being more diverged, the blood-feeding hemipterans have conserved synteny and we detect only two chromosome fusion or fission events. The exceptional rate of structural evolution of aphid autosomes renders them an important emerging model system for studying the role of large-scale genome rearrangements in evolution.

A chromosome-level genome assembly of the woolly apple aphid,Eriosoma lanigerum(Hausmann) (Hemiptera: Aphididae)

“…To create the de novo assembly, the 10X Genomics linked-read data were assembled using Supernova 2.1.1 (Weisenfeld, Kumar, Shah, Church, & Jaffe, 2017) with the default parameters and the recommended number of reads (--maxreads=199222871) to produce the pseudohaplotype assembly output (--style=pseudohap). We improved the initial Supernova assembly by performing iterative scaffolding using all of the 10X Genomics raw data (364 millions of reads; Supplementary Table 1) following the procedure set out in Mathers, Wouters, et al (2020). Briefly, we performed two rounds of Scaff10x (https://github.com/wtsihpag/Scaff10X) with the parameters "-longread 1 -edge 50000 -block 50000", followed by mis-assembly detection and correction with Tigmint (Jackman et al, 2018).…”

“…Orthologous groups in Aphididae genomes were identified from the predicted protein sequences of WAA and nine other aphid genomes already published ( Supplementary Table 3): Myzus cerasi Thorpe et al, 2018), Myzus persicae (Mathers, Wouters, et al, 2020), Diuraphis noxia (Nicholson et al, 2015), Acyrthosiphon pisum (Mathers, Wouters, et al, 2020), Pentalonia nigronervosa , Aphis glycines (Mathers, 2020), Rhopalosiphum maidis (Chen et al, 2019), Rhopalosiphum padi (Thorpe et al, 2018) and Cinara cedri (Julca et al, 2020). As an outgroup, we included the genome of the silverleaf whitefly Bemisia tabaci (Chen et al, 2016).…”

“…While aphid genomics research has mostly focussed on the subfamily Aphidinae (International Aphid Genomics Consortium, 2010;Y. Li, Park, Smith, & Moran, 2019;Mathers, 2020;Mathers et al, 2017;Mathers, Wouters, et al, 2020;Nicholson et al, 2015;Thorpe et al, 2018;Wenger et al, 2016), a large and widespread group including many important pests (Blackman & Eastop, 2000), investigation of genome evolution across the wider diversity of aphids has been limited (but see Julca et al, 2020). This report represents the first complete genome sequence for a species from the Eriosomatinae subfamily which includes three potentially polyphyletic tribes (Eriosomatini, Fordini and Pemphigini), all of which are distantly related to members of Aphidinae (X.…”

Genome sequence of the banana aphid, Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) and its symbionts

“…To investigate the phylogenetic position of P. nigronervosa within aphids we carried out orthology clustering of 223,889 protein sequences from P. nigronervosa, our improved M. cerasi annotation, and seven previously published aphid genomes (Nicholson et al 2015;Thorpe et al 2018;Chen et al 2019;Mathers 2020;Mathers et al 2020). Although the number of aphid species with sequenced genomes is still low, the included species span three aphid tribes (Macrosphini, Aphidini and Lachnini) and approximately 100 million years of aphid evolution (Kim et al 2011;Hardy et al 2015;Julca et al 2019).…”

“…Despite their economic importance, little to no genomic resources exist for many of these species or their relatives, hindering efforts to understand the evolution and ecology of aphid pests. To date, genome sequencing efforts have focused on members of the aphid tribe Macrosiphini (within subfamily Aphidinae), including the widely studied aphids Acyrthosiphon pisum (pea aphid) (IAGC 2010;Li et al 2019;Mathers et al 2020) and Myzus persicae (green peach aphid) (Mathers et al 2017, as well as other important pest species such as Diuraphis noxia (Russian wheat aphid) (Nicholson et al 2015). Recently, additional genome sequences have become available for members of the tribe Aphidini (also in the subfamily Aphidinae) (Wenger et al 2017;Thorpe et al 2018;Chen et al 2019;Quan et al 2019;Mathers 2020) and the subfamily Lanchiniae (Julca et al 2019), broadening the phylogenetic scope of aphid genomic resources.…”