Gene Family Evolution in the Pea Aphid Based on Chromosome-Level Genome Assembly

Abstract

Genome structural variations, including duplications, deletions, insertions, and inversions, are central in the evolution of eukaryotic genomes. However, structural variations present challenges for high-quality genome assembly, hampering efforts to understand the evolution of gene families and genome architecture. An example is the genome of the pea aphid (Acyrthosiphon pisum) for which the current assembly is composed of thousands of short scaffolds, many of which are known to be misassembled. Here, we present an improved version of the A. pisum genome based on the use of two long-range proximity ligation methods. The new assembly contains four long scaffolds (40–170 Mb), corresponding to the three autosomes and the X chromosome of A. pisum, and encompassing 86% of the new assembly. Assembly accuracy is supported by several quality assessments. Using this assembly, we identify the chromosomal locations and relative ages of duplication events, and the locations of horizontally acquired genes. The improved assembly illuminates the mode of gene family evolution by providing proximity information between paralogs. By estimating nucleotide polymorphism and coverage depth from resequencing data, we determined that many short scaffolds not assembling to chromosomes represent hemizygous regions, which are especially frequent on the highly repetitive X chromosome. Aligning the X-linked aphicarus region, responsible for male wing dimorphism, to the new assembly revealed a 50-kb deletion that cosegregates with the winged male phenotype in some clones. These results show that long-range scaffolding methods can substantially improve assemblies of repetitive genomes and facilitate study of gene family evolution and structural variation.

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

“…These two wasps parasitize aphids exclusively, and aphids themselves have relatively low genome-wide GC content, perhaps related to their high-sugar, lownitrogen, sap diet. This includes the pea aphid (Acyrthosiphon pisum, Additional file 6), which is a frequent host of A. ervi and also has notably low GC content (29.8%) [120]. We did not observe a relationship in codon usage nor nitrogen content between wasps and other taxa in this system (i.e.…”

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

“…There are approximately 5,000 known species of aphid (Hemiptera: Aphididae), and approximately 100 of these are of significant agricultural economic importance (Blackman & Eastop, 2017). 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).…”

Functional insights from the GC-poor genomes of two aphid parasitoids,Aphidius erviandLysiphlebus fabarum

“…These two wasps parasitize aphids exclusively, and aphids 249 themselves have relatively low genome-wide GC content. This includes the pea aphid 250 (Acyrtosiphon pisum), which is a frequent host of A. ervi and also has notably low GC 251 content (29.8%, Li et al 2019). This is not limited to A. pisum, with other aphid 252 genomes' GC content ranging between 26.8% -30% (Additional File 2), perhaps related 253 to their high-sugar, low-nitrogen, sap diet.…”