Transposable element expansion and low-level piRNA silencing in grasshoppers may cause genome gigantism

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Abstract

Background

Transposable elements (TEs) have been likened to parasites in the genome that reproduce and move ceaselessly in the host, continuously enlarging the host genome. However, the Piwi-interacting RNA (piRNA) pathway defends animal genomes against the harmful consequences of TE invasion by imposing small-RNA-mediated silencing. Here we compare the TE activity of two grasshopper species with different genome sizes in Acrididae ( Locusta migratoria manilensis♀1C = 6.60 pg, Angaracris rhodopa♀1C = 16.36 pg) to ascertain the influence of piRNAs.

Results

We discovered that repetitive sequences accounted for 74.56% of the genome in A. rhodopa, more than 56.83% in L. migratoria, and the large-genome grasshopper contained a higher TEs proportions. The comparative analysis revealed that 41 TEs (copy number > 500) were shared in both species. The two species exhibited distinct “landscapes” of TE divergence. The TEs outbreaks in the small-genome grasshopper occurred at more ancient times, while the large-genome grasshopper maintains active transposition events in the recent past. Evolutionary history studies on TEs suggest that TEs may be subject to different dynamics and resistances in these two species. We found that TE transcript abundance was higher in the large-genome grasshopper and the TE-derived piRNAs abundance was lower than in the small-genome grasshopper. In addition, we found that the piRNA methylase HENMT, which is underexpressed in the large-genome grasshopper, impedes the piRNA silencing to a lower level.

Conclusions

Our study revealed that the abundance of piRNAs is lower in the gigantic genome grasshopper than in the small genome grasshopper. In addition, the key gene HENMT in the piRNA biogenesis pathway (Ping-Pong cycle) in the gigantic genome grasshopper is underexpressed. We hypothesize that low-level piRNA silencing unbalances the original positive correlation between TEs and piRNAs, and triggers TEs to proliferate out of control, which may be one of the reasons for the gigantism of grasshopper genomes.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12915-022-01441-w.

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Motivation: Although many next-generation sequencing (NGS) read preprocessing tools already existed, we could not find any tool or combination of tools that met our requirements in terms of flexibility, correct handling of paired-end data and high performance. We have developed Trimmomatic as a more flexible and efficient preprocessing tool, which could correctly handle paired-end data. Results: The value of NGS read preprocessing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output that is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested. Availability and implementation: Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available at http://www.usadellab.org/cms/index.php?page=trimmomatic Contact: usadel@bio1.rwth-aachen.de Supplementary information: Supplementary data are available at Bioinformatics online.

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Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data

Manfred Grabherr, Brian Haas, Moran Yassour … (2011)

Massively-parallel cDNA sequencing has opened the way to deep and efficient probing of transcriptomes. Current approaches for transcript reconstruction from such data often rely on aligning reads to a reference genome, and are thus unsuitable for samples with a partial or missing reference genome. Here, we present the Trinity methodology for de novo full-length transcriptome reconstruction, and evaluate it on samples from fission yeast, mouse, and whitefly – an insect whose genome has not yet been sequenced. Trinity fully reconstructs a large fraction of the transcripts present in the data, also reporting alternative splice isoforms and transcripts from recently duplicated genes. In all cases, Trinity performs better than other available de novo transcriptome assembly programs, and its sensitivity is comparable to methods relying on genome alignments. Our approach provides a unified and general solution for transcriptome reconstruction in any sample, especially in the complete absence of a reference genome.

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Author and article information

Contributors

Yuan Huang:

ORCID: http://orcid.org/0000-0001-7683-9193

yuanh@snnu.edu.cn

Journal

Journal ID (nlm-ta): BMC Biol

Journal ID (iso-abbrev): BMC Biol

Title: BMC Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1741-7007

Publication date (Electronic): 28 October 2022

Publication date PMC-release: 28 October 2022

Publication date Collection: 2022

Volume: 20

Electronic Location Identifier: 243

Affiliations

[1 ]GRID grid.412498.2, ISNI 0000 0004 1759 8395, College of Life Sciences, , Shaanxi Normal University, ; Xi’an, China

[2 ]GRID grid.508540.c, ISNI 0000 0004 4914 235X, School of Basic Medical Sciences, , Xi’an Medical University, ; Xi’an, China

[3 ]GRID grid.440740.3, ISNI 0000 0004 1757 7092, College of Life Science and Engineering, , Henan University of Urban Construction, ; Pingdingshan, China

Author information

Yuan Huang http://orcid.org/0000-0001-7683-9193

Article

Publisher ID: 1441

DOI: 10.1186/s12915-022-01441-w

PMC ID: 9615261

PubMed ID: 36307800

SO-VID: 78cdb2d5-818a-4000-9155-0db345d23129

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 24 August 2022

Date accepted : 17 October 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31872217

Award Recipient : Yuan Huang

Funded by: FundRef http://dx.doi.org/10.13039/501100012226, Fundamental Research Funds for the Central Universities;

Award ID: GK202206021,GK202101003

Award Recipient : Yuan Huang

Custom metadata

ScienceOpen disciplines: Life sciences

Keywords: genome size,transposable elements,te transcripts,pirna silencing,grasshopper

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: genome size, transposable elements, te transcripts, pirna silencing, grasshopper

Transposable element expansion and low-level piRNA silencing in grasshoppers may cause genome gigantism

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Abstract

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Supplementary Information

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Genome Integrity

Most cited references 117

Trimmomatic: a flexible trimmer for Illumina sequence data

Cutadapt removes adapter sequences from high-throughput sequencing reads

Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data

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