Transposons and non-coding regions drive the intrafamily differences of genome size in insects

Cong, Yuyang; Ye, Xinhai; Yang, Mei; He, Kang; Li, Fei

doi:10.1016/j.isci.2022.104873

Cited by 21 publications

(15 citation statements)

References 146 publications

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“…Since LTRs are particularly difficult to identify due to their size and complexity (Flynn et al 2020), and because Drosophila LTRs are better characterized in RE databases than other insect lineages (see below), this trend may reflect methodology more than biology. Consistent with previous studies (Cong et al 2022; Heckenhauer et al 2022; Petersen et al 2019), we showed that RE abundance correlates with genome size (Fig. 2j).…”

Section: Resultssupporting

confidence: 93%

“…For example, in caddisflies (Trichoptera), clades containing relatively larger genomes (e.g., 600– 2100 Mb) show higher species diversity and ecological breadth than small-genome lineages (e.g., >600 Mb), raising the potential for adaptive advantages of maintaining high repeat loads (Heckenhauer et al 2022; Olsen et al 2021). While the current study includes assembly lengths up to 4100 Mb, flow cytometry data shows evidence of insect genomes exceeding 18,000 Mb ( Bryodemella holdereri , Cong et al 2022). Insect models have potential to offer new insights on genome gigantism as assemblies for additional large-genome species become available (Liu et al 2022).…”

Section: Discussionmentioning

confidence: 88%

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600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Sproul

Hotaling

Heckenhauer

et al. 2022

Preprint

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Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes. Yet, RE dynamics remain understudied in many taxonomic groups, preventing holistic understanding of how genomes and species evolve. Here, we investigated REs across 601 insect species (20 orders) to better understand the RE landscape of insects and to evaluate automated RE annotation methods in the era of biodiversity genomics. We identified wide variation in the types and frequency of REs across insect groups. We quantified associations between REs and protein-coding genes and found an elevated frequency of associations in insects with abundant long interspersed nuclear elements (LINEs). Sequencing technology impacts RE detection; ~36% more REs could be identified in long-read versus short-read assemblies. Long terminal repeats (LTRs) showed markedly improved detection in long-read assemblies (162% more), while DNA transposons and LINEs showed less respective technology-related bias. We illustrate fundamental challenges to efficient study of REs in diverse groups, showing that in most insect lineages, 25-85% of repetitive sequences were unclassified compared to only ~13% of unclassified repeats in Drosophila species. Our findings suggest this RE-annotation bottleneck, driven largely by uneven taxonomic representation in RE reference databases, is worsening. Although the diversity of available insect genomes has rapidly expanded, the rate of community contributions to RE databases (essential for RE annotation) has not kept pace, preventing high resolution study of REs in most groups. We highlight the tremendous opportunity and need for the field of biodiversity genomics to embrace REs and suggest collective steps for making progress towards this goal.

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Section: Resultssupporting

confidence: 93%

Section: Discussionmentioning

confidence: 88%

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Sproul

Hotaling

Heckenhauer

et al. 2022

Preprint

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“…These results suggest that the compact genomes of chironomids likely evolved in a common ancestor with Ceratopogonidae, although having only one species from Ceratopogonidae in our analysis makes this conclusion less certain. Our results also suggest that the reduction in genome size occurred through non-coding regions and repeat elements, which is consistent with a recent analysis of contributors to insect genome sizes (Cong et al 2022). However, unlike Cong et al (2022), our repeat-element divergence landscapes reveal no obvious connection between repeat element ages and genome size (fig.…”

Section: Resultssupporting

confidence: 93%

Shared features underlying compact genomes and extreme habitat use in chironomid midges

Nell,

Weng,

Phillips

et al. 2023

Preprint

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Non-biting midges (family Chironomidae) are found throughout the world in a diverse array of aquatic and terrestrial habitats, can often tolerate harsh conditions such as hypoxia or desiccation, and have consistently compact genomes. Yet we know little about the shared molecular basis for these attributes and how they have evolved across the family. Here, we address these questions by first creating high-quality, annotated reference assemblies forTanytarsus gracilentus(subfamily Chironominae, tribe Tanytarsini) andParochlus steinenii(subfamily Podonominae). Using these and other publicly available assemblies, we created a time-calibrated phylogenomic tree for family Chironomidae with outgroups from order Diptera. We used this phylogeny to test for features associated with compact genomes, as well as examining patterns of gene family evolution and positive selection that may underlie chironomid habitat tolerances. Our results suggest that compact genomes evolved in the most recent common ancestor of Chironomidae and Ceratopogonidae, and that this occurred mainly through reductions in non-coding regions (introns, intergenic sequences, and repeat elements). Gene families that significantly expanded in Chironomidae included biological processes that may relate to tolerance of stressful environments, such as temperature homeostasis, inflammatory response, melanization defense response, and trehalose transport. We identified a number of genes with evidence for positive selection in Chironomidae, notably sulfonylurea receptor, peroxiredoxin-1, and protein kinase D. Our results help to understand the genomic basis for the small genomes and extreme habitat use in this widely distributed group.Significance StatementChironomid midges are known for having small genomes and being able to tolerate many forms of environmental stress, yet little is known of the shared features of their genomes that may underlie these traits. We found that reductions in non-coding regions coincide with small chironomid genomes, and we identified duplicated and/or selected genes that may equip chironomids to tolerate harsh conditions. These results describe the key genomic changes in chironomid midges that may explain their ability to inhabit a range of extreme habitats across the world.

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“…In addition, we found 2,275 Helitronrelated sequences contributing to 0.88% (22,683,504 bp) of the genome and 1,990 non-coding RNA (ncRNA) genes accounting for 0.012% (312,251 bp) of the genome. Repetitive elements (REs) have repeatedly been shown to be an important driver of genome expansions 46,53,55,56 , but surprisingly contribute to a lower proportion of the D. hillmani genome (37.59%) than expected. This unexpectedly low proportion of REs could be caused by the inability of current RE detection software to detect ancient REs where mutations have accumulated, as has been suggested before 55,57,58 .…”

Section: Structural and Functional Genome Annotationmentioning

confidence: 99%

“…This suggests that there may have been an ancestral largescale genome expansion within the family. Genome size expansions are less common than genome contractions and their evolutionary implications are often not clear [46][47][48][49] , even though they have been suggested to influence host range, reproductive fitness, and morphological traits in different taxa 46,[50][51][52] . Recently, genome size expansions in caddisflies (Trichoptera), the sister taxon of Lepidoptera, were related to more diverse and unstable habitats 53 .…”

Section: Genome Sizes Of Lepidopteramentioning

confidence: 99%

A high-quality genome assembly of the ghost mothDruceiella hillmaniprovides new evidence of genome size augmentation in Hepialidae

Weng,

Lopez-Cacacho,

Foquet

et al. 2023

Preprint

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Ghost moths are an unusual family of primitive moths (Lepidoptera: Hepialidae) known for their large body size and crepuscular adult activity. These moths represent an ancient lineage, frequently have soil dwelling larvae, and are adapted to high elevations, deserts, and other extreme environments. Despite being rather speciose with more than 700 species, there is a dearth of genomic resources for the family. Here, we present the first high quality, publicly available hepialid genome, generated from an Andean species of ghost moth,Druceiella hillmani. Our genome assembly has a length of 2,586 Mbp with contig N50 of 28.1 Mb and N50 of 29, and BUSCO completeness of 97.1%, making it one of the largest genomes in the order Lepidoptera. Our assembly is a vital resource for future research on ghost moth genomics.

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Transposons and non-coding regions drive the intrafamily differences of genome size in insects

Cited by 21 publications

References 146 publications

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Shared features underlying compact genomes and extreme habitat use in chironomid midges

A high-quality genome assembly of the ghost mothDruceiella hillmaniprovides new evidence of genome size augmentation in Hepialidae

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