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. 2024 Dec 2;11:1310. doi: 10.1038/s41597-024-04179-y

Chromosome-level genome assembly of a stored-product psocid, Liposcelis tricolor (Psocodea: Liposcelididae)

Shi-Die Jiang 1, Yu-Ang Chen 1, Sheng-Yuan Sun 1, Guy Smagghe 3,4,5, Jin-Jun Wang 1,2,3, Dan-Dan Wei 1,2,3,✉
PMCID: PMC11612421  PMID: 39622886

Abstract

Liposcelis tricolor (Psocoptera: Liposcelididae) is a significant pest affecting stored products globally. However, due to the lack of a detailed genomic reference, the mechanisms of sex determination, stress resistance, and potential control methods for this booklouse remain poorly understood. In this study, the chromosome-level genome of L. tricolor was assembled by employing Illumina, Nanopore, and Hi-C sequencing technologies. The final genome size was determined to be 229.33 Mb, anchored to 9 pseudo-chromosomes. BUSCO analysis showed that 99.2% of complete BUSCOs were identified, suggesting the high completeness of the genome. A total of 91.49 Mb of repetitive sequences, accounting for 38.84% of the total genome, were annotated, and 15,647 protein-coding genes were predicted, with 88.17% functionally annotated. Additionally, we identified 25 typical sex-determining genes based on the genomic data. This high-quality genome assembly provides a crucial foundation for advancing our comprehension of the molecular biology, genetics, and potential control strategies for psocid L. tricolor.

Subject terms: Entomology, Genome

Background & Summary

Booklice, a stored-product pest of significant economic importance within the order Psocoptera, pose a serious threat to global grain and food security1. In recent years, controlling booklice has become increasingly challenging due to their rapid development of resistance, wide distribution, broad feeding range, ability to transmit pathogens, and strong reproductive capacity2,3. Currently, control of booklice primarily relies on contact insecticides and fumigants. However, under the circumstance of widespread insecticide resistance4–8, there is an urgent need to identify new targets for environmentally friendly control methods. Among the booklice, Liposcelis tricolor is a representative species that is widespread and problematic in China9.

Throughout evolution, insects have developed diverse sex determination systems, each governed by complex internal molecular regulatory mechanisms10,11. The study of these mechanisms has long been a global research focus. While current studies primarily center on model organisms, there is an increasing trend toward leveraging sex-determining genes for pest control12. Genetic engineering interventions aimed at manipulating insect sex for disrupting reproduction offer innovative solutions for pest control. For example, gene-editing technologies such as precision guided sterility insect technology (pgSIT) have been effectively applied to Aedes aegypti, providing a promising strategy for large-scale agricultural pest control13. Meanwhile, comprehensive analysis of sex determination mechanisms in pests could also shed light on their role in the evolution of pest resistance. Interestingly, a unique sex determination pattern, known as paternal genome elimination (PGE), was identified in a booklouse species (Liposcelis sp.)14. However, whether the PGE pattern is widespread in booklice remains to be investigated.

Unfortunately, there is a significant gap in research on the sex determination mechanism in booklice, which hampers the application of emerging technologies like gene drive for their control. As sequencing technology advances, genomic data provide important basic data for entomological research. The assembly of high-quality genomes will be crucial for elucidating the molecular regulatory mechanisms of sex determination in booklice. Within booklice, only the genomes of Liposcelis brunnea15 and Liposcelis bostrychophila16 have been reported to date.

In this study, we used Illumina, Nanopore, and Hi-C sequencing technologies to assemble the chromosome-level genome of L. tricolor. The final genome size was determined to be 229.33 Mb, anchored to 9 pseudo-chromosomes, with a genome integrity of 99.2%. Genome annotation identified 15,647 protein-coding genes, 88.17% of which were functionally annotated. The genome assembly in this study provides a worthy foundation for evolutionary investigation of L. tricolor and the development of novel control strategies.

Methods

Sample collection and sequencing

L. tricolor was collected from a wheat warehouse in Heze, Shandong, China, in 2002 and has since been propagated in the laboratory using artificial diet. In brief, the rearing conditions were maintained at 27.5 ± 0.5 °C, 75–80% relative humidity, and total darkness. The artificial feed was composed of whole wheat flour, yeast powder, and skimmed milk powder in a ratio of 10:1:1.

Genomic DNA was extracted from approximately 1,000 female adults of L. tricolor using the Qiagen DNeasy extraction Kit (Qiagen, cat. Nos. 69504). For short-read sequencing, a 350 bp paired-end Illumina library was prepared and then sequenced on an Illumina NovaSeq platform (Illumina, CA, USA). For Nanopore sequencing, a large-insert (>10 kb) library was prepared following the protocol provided by the manufacturer and sequenced using the PromethION sequencer (Oxford Nanopore). For Hi-C sequencing, we constructed the Hi-C library according to the standard protocol17 and sequenced on the Illumina HiSeq platform at Novogene Science and Technology Co., Ltd (Beijing, China). After removing the low-quality sequences, we obtained 40.33 Gb (183.19×) Illumina data, 43.83 Gb (186.09×) Nanopore data, and 27.41 Gb (119.52×) of the Hi-C data (Table 1). Total RNA was extracted from 500 adults of L. tricolor using the TRIzol reagent (Invitrogen, MA, USA). RNA-seq libraries for conventional transcriptome sequencing were constructed by Biomarker Technologies (Beijing, China) and then sequenced on the Illumina HiSeq 2000 platform, yielding 2.50 Gb of 150-bp paired-end reads (Table 1). For full-length transcriptome sequencing, RNA-seq libraries were generated by Novogene Science and Technology Co., Ltd (Beijing, China) using the SMRTbell™ Template Prep Kit 1.0 (Pacific Biosciences, USA). Sequencing was conducted on the PacBio Sequel II platform, resulting in 10.00 Gb of RNA-Seq data (Table 1).

Table 1.

Statistics for the sequencing data of L. tricolor genome.

Library Clean data(Gb) Coverage(X) Usage
Illumina 40.33 183.19 Genome survey
Nanopore 43.83 186.09 Scaffold assembly
Hi-C 27.41 119.52 Chromosome assembly
Illumina RNA-Seq 2.50 Gene structure annotation
Pacbio RNA-Seq 10.00 Gene structure annotation
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Genome feature estimation

The short Illumina reads were quality-filtered by fastp18 with the parameters ‘-q 10 -u 50 -y -g -Y 10 -e 20 -l 100 -b 150 -B 150’ and then used for genome survey. We performed K-mer counting (k = 19) by Jellyfish (v2.2.10)19 and calculated genome characteristics with Genomescope (v2.0)20. The genome size of L. tricolor was estimated to be 220.15 Mb, with 24.94% repeat sequence content and 0.36% heterozygosity (Table 2; Fig. 1A).

Table 2.

Statistics for L. tricolor genome assembly.

Type Item Feature
Genome survey Genome size (Mb) 220.15
Heterozygosity 0.36%
GC content 33.64%
Assembled genome Genome size (Mb) 229.33
Chromosome number 9
Contig number 110
Contig N50 (Mb) 13.12
GC content 33.90%
BUSCO completeness C:99.2% [S:98.0%, D:1.2%], F:0.5%, M:0.3%, n:1013
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Fig. 1.

Fig. 1

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Overview of the L. tricolor genome assembly and features. (A) GenomeScope estimation of genome size and heterogeneity using a k-mer of 19. (B) HI-C interactive heat map of L. tricolor. (C) Circos plot of the linkage groups. From outside to inside, it is chromosome length, GC content, and gene density. (D) BUSCO assessment of genome assembly integrity.

Draft Genome assembly and chromosome assembly

The long reads from Nanopore were used to assemble a contig-level genome of L. tricolor. After filtering adapters and low-quality reads, the data were error-corrected with Canu (v1.7.1)21 and assembled using Smartdenovo22 with default parameters. Pilon (v1.22)23 was then employed for three rounds of polishing, followed by final error correction using short reads from Illumina. The resulting draft genome was 235.54 Mb in size, consisting 110 contigs with a contig N50 of 13.12 Mb (Table 2).

The chromosome-level genome of L. tricolor was assembled using Hi-C sequencing data. After cleaning, the Hi-C reads were aligned to the contigs by Juicer (v1.9.9)24 and then 110 contigs were anchored to pseudo-chromosomes using 3D-DNA25. Manual corrections were made using Juicebox (v1.11.08)26. This process successfully anchored the L. tricolor genome into 9 pseudo-chromosomes, with a final genome size was 229.33 Mb (Table 2; Fig. 1B,C). Genome completeness was assessed using BUSCO (v5.4.5)27 with both the arthropoda_odb10 database and insecta OrthoDB v10 database. The results demonstrated that 99.2% and 98.76% of complete BUSCOs were included in this assembly, respectively (Table 2; Fig. 1D; Supplementary Table S1).

Repeat annotation and gene prediction

Transposon elements (TEs) were annotated using homology-based and de novo approaches. First, RepeatModeler (v2.0.3)28, RECON (v1.08)29, RepeatScout (v1.05)30, LTR_retriever (v2.8)31 and LTR_finder (v1.07)32 were used to customize a de novo repeat library. The repeat libraries were then categorized using RepeatClassifier (v1.0)33. By merging the de novo TE sequences library with the existing databases, including Repbase (v19.06)34, REXdb (v3.0)35 and Dfam (v3.2)36, a non-redundant species-specific TE library was constructed. RepeatMasker (v4.10)37 was finally employed to identify and classify the TE sequences in the L. tricolor genome. In total, 91.49 Mb repeat sequences were identified, representing 38.84% of the assembled L. tricolor genome (Table 3). Among these, 59.33 Mb were TE sequences, representing 25.19% of the genome, and 32.16 Mb were tandem repeats, accounting for 13.65% of the assembled L. tricolor genome. Additionally, the proportion of repeat sequences in the L. tricolor genome (38.84%) exhibited a higher similarity with L. bostrychophila (37.88%)16, compared to L. brunnea (15.9%)15.

Table 3.

Statistics of repeat sequences information in L. tricolor genome.

Repeat type Sequence type number Total length /bp Percentage/%
Transposable elements ClassI:Retroelement 105,510 22,770,499 9.67
ClassI/DIRS 788 94,560 0.04
ClassI/LINE 18,423 4,251,852 1.81
ClassI/LTR/Cassandra 4 238 0.00
ClassI/LTR/Caulimovirus 13 852 0.00
ClassI/LTR/Copia 1,498 508,694 0.22
ClassI/LTR/ERV 19,853 5,159,655 2.19
ClassI/LTR/Gypsy 7,958 2,342,537 0.99
ClassI/LTR/Pao 891 274,255 0.12
ClassI/LTR/Unknown 52,632 9,576,286 4.07
ClassI/LTR/Viper 10 2,369 0.00
ClassI/SINE 3,440 559,201 0.24
ClassII:DNA transposon 172,286 36,557,336 15.52
ClassII/Academ 23 3,234 0.00
ClassII/CACTA 5,738 1,079,952 0.46
ClassII/Crypton 271 65,746 0.03
ClassII/Dada 205 47,657 0.02
ClassII/Ginger 171 52,455 0.02
ClassII/Helitron 23,031 5,315,165 2.26
ClassII/IS3EU 3,576 1,269,943 0.54
ClassII/Kolobok 200 13,602 0.01
ClassII/MITE 31 4,420 0.00
ClassII/Maverick 497 276,841 0.12
ClassII/Merlin 330 62,240 0.03
ClassII/Mutator 1,491 201,718 0.09
ClassII/Novosib 61 3,826 0.00
ClassII/P 86 6,499 0.00
ClassII/PIF-Harbinger 799 89,620 0.04
ClassII/PiggyBac 484 133,110 0.06
ClassII/Sola 74 4,794 0.00
ClassII/Tc1-Mariner 2,593 818,468 0.35
ClassII/Unknown 112,725 23,551,799 10.00
ClassII/Zator 2,794 444,190 0.19
ClassII/Zisupton 63 4,942 0.00
ClassII/hAT 17,043 3,107,115 1.32
Tandem repeats microsatellite(1–9 bp units) 360,331 7,054,330 3.00
minisatellite(10–99 bp units) 10,699 16,041,633 6.81
satellite(>=100 bp units) 8,162 9,061,682 3.85
Total 656,988 91,485,480 38.84
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A thorough method was used to identify protein-coding genes in the L. tricolor genome, combining de novo prediction, homology search, and Unigenes from the transcriptome. De novo predictions were made by Augustus (v2.4)38 and SNAP (v2006-07-28)39. For the homolog-based searching, GeMoMa (v1.7)40 was employed using reference gene models from four other species (Acyrthosiphon pisum, Drosophila melanogaster, L. bostrychophila, and Pediculus humanus). Unigene prediction was carried out using PASA (v2.0.2)41 to predict genes based on the Unigene assemblies without reference. Gene models generated from these diverse methods were consolidated by Evidence Modeler (EVM) (v1.1.1)42 and further refined with PASA (v2.0.2)41. The predicted gene sequences were functionally annotated by searching the Gene Ontology (GO)43, Kyoto Encyclopedia of Genes and Genomes (KEGG)44, eukaryotic orthologous groups (KOG)45, Pfam46, SwissProt47, TrEMBL48, eggNOG49, and GenBank Non-Redundant (NR) databases50. In total, 15,647 protein-coding genes (PCGs) were annotated (Table 4), with 88.17% (13,796 genes) having functional annotations in the L. tricolor genome (Table 5).

Table 4.

Statistics of gene prediction results.

Method of prediction Software Species Gene number
Ab initio Augustus — 16,542
SNAP — 35,016
Homology-based GeMoMa Acyrthosiphon pisum 10,802
Drosophila melanogaster 9,454
Liposcelis bostrychophila 10,420
Pediculus humanus 11,034
RNAseq GeneMarkS-T — 12,926
PASA — 12,306
Integration EVM — 15,647
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Table 5.

Gene function annotation statistics information.

Annotation database Number of annotated genes Proportion of annotated genes /%
GO_Annotation 11,904 76.08
KEGG_Annotation 11,795 75.38
KOG_Annotation 10,380 66.34
Pfam_Annotation 12,922 82.58
Swissprot_Annotation 11,716 74.88
TrEMBL_Annotation 11,654 74.48
EggNOG_Annotation 10,358 66.20
Nr_Annotation 11,862 75.81
All_Annotated 13,796 88.17
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Synteny analysis

Synteny analysis of the chromosome-level genomes of L. tricolor, L. bostrychophila, and L. brunnea was conducted using TBtools51. The analysis employed the One Step MCScanX plugin for synteny detection, the Fasta Stats plugin for chromosome backbones generation, and the multiple synteny plot plugin for visualization. The results revealed several instances of chromosome fusion and division among the three species. The L. tricolor genome exhibited a higher degree of chromosomal synteny with L. bostrychophila compared to L. brunnea (Fig. 2). Specifically, except for chr9 of L. bostrychophila, which was not aligned, chr8 and 9 of L. tricolor corresponded to chr6 of L. bostrychophila, while the remaining chromosomes showed good collinearity and matched one-to-one.

Fig. 2.

Fig. 2

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Syntenic analysis. (A) Synteny blocks between L. tricolor and L. bostrychophila (LBOS). (B) Synteny blocks between L. tricolor and L. brunnea (LBRU).

Sex-determining genes in L. tricolor

Based on the classification of “sex determination” in the NCBI BioSystem database, 30 insect sex determination genes were identified52. These genes are shown to regulate sex determination in model insects such as D. melanogaster and B. mori53,54. The amino acid sequences of the corresponding genes from D. melanogaster and B. mori were downloaded from the NCBI database and used as query sequences. Local BLAST searches were performed against the L. tricolor genome and transcriptome sequences, initially with a threshold of E-value < 10−5. If no matches were found, the threshold was adjusted to 0.01 and BLAST was repeated to ensure no genes were missed. Following this, target sequences were manually inspected, and their conserved structural domains were analyzed using NCBI CD-search55. Molecular characterization parameters, such as molecular weight and isoelectric point, were calculated using the Expasy ProtParam tool56.

A total of 25 typical insect sex-determining genes were identified in the L. tricolor genome and transcriptome (Supplementary Table S2). These include genes involved in the somatic cell sex determination pathway: da, dpn, dsf, dsx, emc, fl(2)d, fru, gro, Imp, ix, PSI, run, snf, Sxl, tra-2, and vir; Dose-compensated genes included mle, mof, msl-1, msl-2, and msl-3. Genes involved in germline sex determination are otu, ovo, stat92E, and hop. Chromosomal localization showed that 25 sex-determining genes are distributed across chr1, 2, 3, 5, 6 and 8 of L. tricolor, with the highest concentration on chr1, which contains 8 genes.

Data Records

All sequencing data has been uploaded to the NCBI SRA database: transcriptomic sequencing data (SRR3033784957 and SRR3034706558), Illumina sequencing data (SRR3015973559), Nanopore sequencing data (SRR3016752660-SRR3016753361–67), and Hi-C sequencing data (SRR3016922868). The chromosome assembly is available in the GenBank database under the accession JBGGLZ00000000069. The genome annotations have been deposited in the Figshare database70.

Technical Validation

Evaluation of the genome assembly

First, the quality of the L. tricolor assembly was evaluated using BUSCO (v5.4.5)27 with arthropoda_odb10 and the insecta OrthoDB v10 databases, identifying 99.2% and 98.76% of the complete BUSCO genes, respectively (Table 2; Fig. 1D; Supplementary Table S1). Additionally, BWA (v0.7.15)71 was employed to map Illumina short reads onto the assembled genome. Of these, 99.24% were aligned to the genome, with 97.58% properly mapped (Supplementary Table S3). These statistics indicated a high level completeness and accuracy of the L. tricolor genome assembly.

Evaluation of the genome annotation

BUSCO (v5.4.5)27 with vertebrata database was employed to assess the completeness of the L. tricolor genome annotation. The analysis indicated that 96.12% of conserved orthologous genes were complete in the predicted PCGs, comprising 93.42% single-copy and 2.71% duplicated genes (Supplementary Table S4).

Supplementary information

Supplementary Tables (186.7KB, pdf)

Acknowledgements

This study received funding from the National Natural Science Foundation of China (32272528) and the Natural Science Foundation of Chongqing (CSTB2024NSCQ-MSX0374).

Author contributions

S.D.J. and D.D.W. coordinated the study and participated in its design. S.D.J., Y.A.C. and S.Y.S. performed experiments, analyzed the data and generated the figures. S.D.J. wrote the first draft of the manuscript. G.S., J.J.W. and D.D.W. revised and edited the manuscript. All authors read and approved the final manuscript.

Code availability

The versions of all software used in this study, along with their parameters, are detailed in the Methods section. The default parameters were utilized for software without detailed parameters. No custom code was employed in the generation or processing of the data described.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

The online version contains supplementary material available at 10.1038/s41597-024-04179-y.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. NCBI Sequence Read Archivehttps://identifiers.org/ncbi/insdc.sra:SRR30337849 (2024).
  2. NCBI Sequence Read Archivehttps://identifiers.org/ncbi/insdc.sra:SRR30347065 (2024).
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  7. NCBI Sequence Read Archivehttps://identifiers.org/ncbi/insdc.sra:SRR30167529 (2024).
  8. NCBI Sequence Read Archivehttps://identifiers.org/ncbi/insdc.sra:SRR30167530 (2024).
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  11. NCBI Sequence Read Archivehttps://identifiers.org/ncbi/insdc.sra:SRR30167533 (2024).
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  13. Jiang, S. D. Genome structure annotation of Liposcelis tricolor. figshare10.6084/m9.figshare.26526388.v1 (2024).

Supplementary Materials

Supplementary Tables (186.7KB, pdf)

Data Availability Statement

The versions of all software used in this study, along with their parameters, are detailed in the Methods section. The default parameters were utilized for software without detailed parameters. No custom code was employed in the generation or processing of the data described.

Articles from Scientific Data are provided here courtesy of Nature Publishing Group

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