Too much too many: comparative analysis of morabine grasshopper genomes reveals highly abundant transposable elements and rapidly proliferating satellite DNA repeats

Abstract

Background: The repeatome, the collection of repetitive DNA sequences represented by transposable elements (TEs) and tandemly repeated satellite DNA (satDNAs), is found in high proportion in organisms across the tree of life. Grasshoppers have large genomes (average 9 Gb), containing large amounts of repetitive DNA which has hampered progress in assembling reference genomes. Here we combined linked-read genomics with transcriptomics to assemble, characterize, and compare the structure of the repeatome and its contribution to genome evolution, in four chromosomal races of the morabine grasshopper Vandiemenella viatica species complex. Results: We obtained linked-read genome assemblies of 2.73-3.27 Gb from estimated genome sizes of 4.26-5.07 Gb DNA per haploid genome of the four chromosomal races of V. viatica. These constitute the third largest insect genomes assembled so far (the largest being two locust grasshoppers). Combining complementary annotation tools and manual curation, we found a large diversity of TEs and satDNAs constituting 66 to 75 % per genome assembly. A comparison of sequence divergence within the TE classes revealed massive accumulation of recent TEs in all four races (314-463 Mb per assembly), indicating that their large genome size is likely due to similar rates of TE accumulation across the four races. Transcriptome sequencing showed more biased TE expression in reproductive tissues than somatic tissues, implying permissive transcription in gametogenesis. Out of 129 satDNA families, 102 satDNA families were shared among the four chromosomal races, which likely represent a repertoire of satDNA families in the ancestor of the V. viatica chromosomal races. Notably, 50 of these shared satDNA families underwent differential proliferation since the recent diversification of the V. viatica species complex. Conclusion: In-depth annotation of the repeatome in morabine grasshoppers provided new insights into the genome evolution of Orthoptera. Our TEs analysis revealed a massive recent accumulation of TEs equivalent to the size of entire Drosophila genomes, which likely explains the large genome sizes in grasshoppers. Although the TE and satDNA repertoires were rather similar between races, the patterns of TE expression and satDNA proliferation suggest rapid evolution of grasshopper genomes on recent timescales.

The transposable element-rich genome of the cereal pestSitophilus oryzae

“…The TE-rich grasshopper L. migratoria repeatome comprises only 14% of DNA transposons, while LINE retroelements (Class I) amount to 25%. Morabine grasshoppers, with up to 75% of TE content, show equivalent amounts of DNA, LINE and Helitrons (Palacios-Gimenez et al 2020). Finally, among Coleoptera, a large diversity of repeatomes is observed (Figure 2C) with A. planipennis, Leptinotarsa decemlineata and Onthophagus taurus carrying an abundant LINE content, while S. oryzae, T. castaneum and Anoplophora glabripennis show larger DNA transposon content.…”

“…From TE-rich genomes as maize (85% (Schnable et al 2009)), humans (≈45% (Lander et al 2001)), and the recently sequenced lungfish (≈90% (Meyer et al 2021)) for instance, to TE-poor genomes, as D. melanogaster (12-15% (Adams et al 2000)), or Arabidopsis thaliana (≈10% (The Arabidopsis Genome Initiative 2000)), repeatomes thrive on a high level of diversity. These drastic variations are also observed within animal clades, such as insects, where the proportion of TE ranges from 2% in the Antarctic midge ( Belgica antarctica ) to 65% in the migratory locust ( Locusta migratoria ) (Petersen et al 2019; Wang et al 2014; Kelley et al 2014) and up to 75% in morabine grasshoppers ( Vandiemenella viatica species) (Palacios-Gimenez et al 2020). In addition to the overall TE content, the number of different TE families (homogeneous groups of phylogenetically related TE sequences), their size (number of copies per family) and sequence diversity are also very high among insect species (Gilbert et al 2021).…”

“…Aedes aegypti and Ae. albopictus 40-50% (Goubert et al 2015; Nene et al 2007), L. migratoria 60-65% (Wang et al 2014; Petersen et al 2019), Dendrolimus punctatus 56% (Zhang et al 2020), Vandiemenella viatica species 66-75% (Palacios-Gimenez et al 2020)).…”

An endangered flightless grasshopper with strong genetic structure maintains population genetic variation despite extensive habitat loss

“…Implicit fragment size selection and next‐generation sequencing of representations are subsequently performed with HiSeq2000 (Illumina) (Georges et al., 2018; Kilian et al., 2012). This technology was considered appropriate for K. scurra to overcome sequencing problems associated with large genomes and high levels of repetitive DNA, gene duplications, and pseudogenes which were expected in this orthopteran species (e.g., Palacios‐Gimenez et al., 2020; Wang et al., 2014).…”

When and how do sex‐linked regions become sex chromosomes?

“…Prominent accumulation of repetitive sequences is detected in recently evolved Drosophila neo‐Y chromosomes (Bachtrog 2003), grasshopper neo‐Y‐linked regions (Palacios‐Gimenez et al. 2020), and before loss of genes in plants including papaya (Wang et al. 2012), and in lizards (Matsubara et al.…”