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. 2026 Jan 23;13:293. doi: 10.1038/s41597-026-06617-5

Transcriptomic Resource of Trissolcus cultratus: A Key Biological Control Agent for Halyomorpha halys

Feng-Qi Li 1, Yong-Zhi Zhong 2,3, Tim Haye 2,4, Francesco Tortorici 5, Sofia Victoria Prieto 5, Li Wang 1,2, Zi-Jian Song 2, Jin-Ping Zhang 2,✉
PMCID: PMC12932653  PMID: 41577701

Abstract

Trissolcus cultratus, a parasitoid wasp of brown marmorated stink bug (BMSB), exhibits divergent parasitic capacities between Chinese and Swiss populations, with Chinese strains successfully reproducing on fresh and cold storage host eggs in both laboratory and field conditions, while Swiss strains fail to develop in fresh BMSB egg. We sequenced and assembled the first T. cultratus transcriptome, a total of 184,932,102 and 195,101,432 clean reads from the Chinese and Swiss strains, respectively, were de novo assembled into 19,280 and 16,322 unigenes. These assemblies predicted 9,811 and 9,582 protein-coding genes for the two strains. Among the 19,280 and 16,322 unigenes, we further identified 554 and 557 transcription factors in the Chinese and Swiss strains, respectively. This work presents the first transcriptomic dataset for T. cultratus, offering a valuable foundation for subsequent research on its population genetics.

Subject terms: Invasive species, Molecular evolution

Background & Summary

The brown marmorated stink bug (BMSB), Halyomopha halys (Stål) (Hemiptera, Pentatomidae), is native to East Asia. It is now invasive worldwide, except in Oceania and Antarctica. BMSB causes significant damage to agricultural and forestry plants1. One factor why BMSB has rapidly evolved into a major pest in newly invaded territories is the lack of control by natural enemies2. In Beijing, China, BMSB eggs are attacked by several egg parasitoids (Hymenoptera) in mixed orchard and mountainous natural habitats, including Trissolcus cultratus (Mayr) (Hym. Scelionidae)3. In addition, T. cultratus and T. japonicus (Ashmead) were confirmed as the two predominant egg parasitoids of BMSB in kiwi orchards4. Swiss populations of T. cultratus frequently parasitize and develop on sentinel frozen eggs of BMSB when exposed in the Swiss Jura mountains5,6. However, development occurred in only 4.2% on fresh BMSB eggs6. Competition tests between Chinese population of T. cultratus and T. japonicus confirmed the intrinsic competitive superiority of the former7. This also occurs in a biologically distinct European population of T. cultratus, suggesting that, in contrast, facultative hyperparasitism is retained in geographically separated populations that have not coevolved with BMSB8.

As the Chinese and Swiss populations have been geographically separated for a long time, biological differences have probably developed between them. Currently, transcriptome or genome resources are not available for T. cultratus, even though such data would deepen our understanding of the observed biological differences between the two strains. The current state of transcriptome data of T. cultratus is notably limited, which constrains our understanding of the molecular evolution and population differentiation mechanisms of this parasitoid wasp.

The objectives of our study were to characterize the female transcriptome dataset of the wasp T. cultratus. Transcriptome sequencing was performed using the Illumina NovaSeq 6000 platform. After filtering out low-quality reads, a total of 184,932,102 and 195,101,432 clean reads from the Chinese and Swiss strains, respectively, were de novo assembled, resulting in 19,280 and 16,322 unigenes. Among these, 9,159 unigenes in the Chinese strain and 9,080 in the Swiss strain were successfully annotated through significant BLASTx matches against the non-redundant (NR), SwissProt, Protein family (Pfam), Clusters of Orthologous Groups (COG), Gene Ontology (GO), and Kyoto Encyclopedia of Genes and Genomes (KEGG) databases. This comprehensive transcriptomic resource for T. cultratus provides valuable insights into the molecular basis underlying variation in parasitic ability.

Methods

Insect materials and RNA isolation

The Chinese colony of T. cultratus was collected from parasitized BMSB eggs in the field in Beijing, China (N 40°02′06″, E 116°12′41″) in 2020. The colony was maintained in acrylic ventilated cages (30 × 30 × 30 cm) and fed on 20% honey water in a rearing room at 25 ± 1 °C, 60 ± 5% RH and16 h Light: 8 h Dark conditions. Parasitoids were provided with fresh BMSB eggs to maintain colonies.

The Swiss strain of T. cultratus was collected in an urban park in Basel, Switzerland (N 47°33′08″, E 7°35′57″) by exposing frozen sentinel BMSB eggs in 2022, that were collected after five days and then reared in the laboratory. Egg masses were kept individually in small Petri-dishes (d = 5 cm) under the same temperature, humidity, and light conditions described previously until all insects had emerged. The conspecific of the two populations was confirmed through morphological analyses using the key proposed by Talamas et al.9 To further validate population assignment, the mitochondrial COI gene was extracted from the transcriptome data of both populations. This molecular check confirms that the Chinese and Swiss SRA datasets correspond to the correct populations.

For both the Chinese and Swiss strains, three-day old mated females were used for the molecular analysis. Three independent biological replicates were established for each tissue sample collection. Each type of tissue (head, thorax, and abdomen) sample was collected from 200 female individuals as a biological replicate. The tissues were frozen in liquid nitrogen and stored at −80 °C. The Trizol technique was employed for the extraction of total RNA, and an Agilent 2100 bioanalyzer (Agilent Technologies, Santa Clara, CA, USA) was used to ascertain both the total quantity and the integrity of the extracted RNA. Transcriptome sequencing was performed separately for both the Chinese and Swiss populations.

cDNA Library Preparation and Illumina Sequencing

The eukaryotic mRNA was enriched using magnetic beads and Oligo (dT) in accordance with the instructions provided in the NEBNext® UltraTM RNA Library Prep Kit for Illumina® (NEB, Ipswich, MA, USA), following an initial evaluation of the quality of the sample RNA. Subsequently, fragmentation buffer was added to facilitate the splitting of the mRNA into short segments. A six-base random primer (random hexamer) was employed to generate single-stranded cDNA using mRNA as template. Afterwards, buffer, dNTPs, DNA polymerase I and RNase H were added to create two-strand cDNA. The AMPure XP beads were employed for the purification of double-stranded cDNA.

The isolated double-stranded cDNA was subjected to A-tailing, repair, and attachment to the sequencing adapter. The AMPure XP system (Beckman Coulter, Beverly, MA, USA) was employed for the purification of the library fragments, with the objective of selecting cDNA fragments that were preferentially 250–300 bp in length. Subsequently, the size-selected, adaptor-ligated cDNA was treated with 3 µL USER Enzyme (NEB, Ipswich, MA, USA) at 37 °C for 15 minutes, followed by a 5-minute incubation at 95 °C prior to PCR. Subsequently, Phusion High-Fidelity DNA Polymerase, Universal PCR Primers, and Index (X) Primers were employed for the purpose of conducting a polymerase chain reaction (PCR). Subsequently, the AMPure XP system was employed for the purification of the PCR products, while the Agilent Bioanalyzer 2100 system was utilized for the assessment of the quality of the libraries. Each RNA sample was subjected to sequencing on the Illumina NovaSeq. 6000 platform, resulting in the generation of 150 bp paired-end reads.

Bioinformatics analysis

The raw data were subjected to filtration using the fastp software (version 0.23.4)10 in order to remove low-quality bases and N bases, thus providing clean reads. The clean reads were then assembled to produce the transcript sequence using the paired-end assembly technique of Trinity v2.6.611. An additional hierarchical clustering phase was conducted using Corset version 4.612 to enhance the final transcriptome dataset. The final transcriptome sequences were evaluated for quality using BUSCO version 5.5.013. Gene function annotations were performed using BLAST with an E-value cutoff of <10−5 in seven primary databases: Nr, Nt, Pfam14, KOG/COG, Swiss-Prot, KEGG, and GO15. Transcription factor identification was conducted using the Animal Transcription Factor Database (version 4.0)16, based on the Pfam files of the transcription factor families. The transcription factor families were identified using hmmsearch17, based on their Pfam files.

Protein-coding sequence (CDS) prediction

The process of CDS prediction is comprised of two distinct stages. The Unigene alignment was conducted in accordance with the established priority order of the NR protein library and the Swiss-Prot protein library using Diamond (v0.9.29) with an E-value cutoff of 1e-5. A comparison of the transcript’s open reading frame (ORF) coding frame information was conducted to extract the relevant data. Subsequently, the coding region sequence was translated into an amino acid sequence (in the order of 5′->3′) using the standard codon table. In the event that a sequence was not matched to either the NR protein library or the Swissprot protein library, or if a sequence was not predicted from the matching results, the TransDecoder (3.0.1)18 was employed to predict the ORFs with default parameters. Only the longest ORF per transcript was retained as the candidate CDS. The final output included both nucleotide sequences and their corresponding amino acid sequences.

Data Records

Raw reads from both the Chinese and Swiss T. cultratus populations have been deposited in the NCBI Sequence Read Archive (SRA) (BioProject ID PRJNA863046)19. The final unigene assembly has been deposited in NCBI GenBank (accession GLGY00000000 for the Chinese T. cultratus strain, and GLKP00000000 for the Swiss T. cultratus strain)20,21. The transcriptome unigenes files can be found in the Figshare22.

Technical Validation

From the T. cultratus female transcriptome, 50,857 and 42,307 transcripts were generated for the Chinese and Swiss strains, respectively (Table 1). The mean quality value, or Q20 score, exceeded 94.68% (Table S1). Furthermore, the combined reads yielded 19,280 and 16,322 unigenes with total lengths of 44,292,959 and 39,245,541 base pairs for the Chinese and Swiss strains, respectively (Table 1). The mean lengths of these unigenes were 2,297 and 2,404 bp, and the corresponding N50 values were 6,202 and 5,650 bp for the Chinese and Swiss strains, respectively (Table 1). Moreover, the size distribution study revealed that 8,069 and 7,810 unigenes were longer than 1,000 bp for the Chinese and Swiss strains, respectively.

Table 1.

Assembly statistics of Trissolcus cultratus transcriptome data.

Type Chinese strain Swiss strain
Total transcripts number 50,857 42,307
Total unigenes number 19,280 16,322
Total sequence base of transcripts 212,196,722 164,984,502
Total sequence base of unigenes 44,292,959 39,245,541
Largest length of transcripts 42,373 40,892
Smallest length of transcripts 301 301
Average lengthof transcripts 4,172 3,900
N50 of transcripts 8,016 7,255
N90 of transcripts 2,306 2,075
Largest length of unigenes 42,373 40,892
Smallest length of unigenes 301 301
Average length of unigenes 2,297 2,404
N50 of unigenes 6,202 5,650
N90 of unigenes 734 850
BUSCO score C:98.7% [S:37.9%, D:60.8%] C:98.8% [S:32.1%, D:66.6%]
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A total of 9,159 and 9,080 unigenes, representing 47.5% and 55.63% of the assemblies, were correctly annotated in at least one database for the Chinese and Swiss strains, respectively. As summarized in Table 2, the NR database exhibited the highest percentage of annotations within a single database (39.43% for the Chinese strains and 47.43% for the Swiss strains), followed by Pfam (38.5% and 44.65%) and GO (38.49% and 44.64%). A comparison of the distribution of the principal species with the NR database revealed that the sequences of Cephus cinctus Norton (14.4%) and Orussus abietinus (Scopoli) (7.2%) exhibited a high degree of similarity to T. cultratus unigenes of the Chinese strain. Conversely, 66.0% of the T. cultratus unigenes sequences exhibit significant similarity to those of other species (Fig. 1Aa). For the Swiss strain, the sequences of Orussus abietinus (Scopoli) (8.6%) and Nasonia vitripennis (6.38%) exhibited a high degree of similarity to T. cultratus unigenes of the Swiss strain. Conversely, 73.2% of the T. cultratus unigenes sequences exhibit significant similarity to those of other species (Fig. 1Ba). According to the E-value distributions (Fig. 1Ab,Bb) of T. cultratus unigenes, 80.2% and 83.0% of the annotated unigenes from the Chinese and Swiss strains, respectively, exhibited considerable homology (E-values < 1e-30) to other sequences in the NR database. As illustrated in Fig. 1Ac, the similarity distributions of the Chinese strain revealed that 18.5% of the sequences exhibited a similarity range of 40% to 60%, while 81.1% of the sequences demonstrated a similarity of over 60%. Similarly, in the Swiss strain, 18.8% of unigenes showed 40–60% sequence identity, and 80.7% exceeded 60% identity (Fig. 1Bc).

Table 2.

Summary of functional annotations of Trissolcus cultratus unigenes.

Database Chinese strain Swiss strain
Number of Unigenes Percentage (%) Number of Unigenes Percentage (%)
Annotated in NR 7,603 39.43 7,742 47.43
Annotated in NT 3,865 20.04 4,337 26.57
Annotated in KO 4,099 21.26 4,226 25.89
Annotated in SwissProt 6,013 31.18 6,349 38.89
Annotated in PFAM 7,423 38.5 7,289 44.65
Annotated in GO 7,421 38.49 7,287 44.64
Annotated in KOG 4,041 20.95 4,332 26.54
Annotated in all Databases 1,935 10.03 2,065 12.65
Annotated in at least one Database 9,159 47.5 9,080 55.63
Total Unigenes 19,280 100 16,322 100
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Fig. 1.

Fig. 1

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Pie charts displaying the distribution of the transcriptome unigenes of Trissolcus cultratus BLASTx matches to the NR database. A mean Chinese strains and B mean Swiss strain. (a) Classification of Species; (b) Distribution of E-values; and (c) Distribution of Similarity.

A total of 7,421 and 7,287 functional annotations with GO functions were acquired from the Chinese and Swiss strains, respectively (Fig. 2). In the Chinese strain, the majority of these annotations pertained to molecular functions (5,124), while the least represented categories were biological processes (5,497) and cellular components (3,530). The most prevalent types of biological processes were cellular process. In the category of cellular components, the most prevalent categories were intracellular terms and cellular anatomical entities. With regard to molecular function, the unigenes were predominantly associated with roles pertaining to binding and catalytic activity (Fig. 2A). A similar GO distribution pattern was observed in the Swiss strain. Most annotations were assigned to molecular functions (4,970), followed by biological processes (5,284) and cellular components (3,435). Cellular processes were the most prevalent biological process terms, whereas intracellular terms and cellular anatomical entities dominated the cellular component category. In the molecular function category, binding and catalytic activity again represented the major functional classes (Fig. 2B).

Fig. 2.

Fig. 2

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GO Classification of Trissolcus cultratus unigenes according to the categories of biological process, Molecular function, and Cellular component. A mean Chinese strains and B mean Swiss strain.

A total of 4,041 and 4,332 annotated putative proteins from the Chinese and Swiss strains, respectively, were assigned to 26 categories based on the function prediction of all unigenes using the KOG-based database. In both strains, the categories in question were primarily as follows: (O) posttranslational modification, protein turnover and chaperones, (R) general function prediction only, and (T) signal transduction mechanisms (Fig. 3A,B). Following the KEGG pathways analysis, 279 KEGG pathways were assigned to 4,251 and 4,461 proteins in the Chinese and Swiss strains, respectively. Signal transduction was the most represented pathway in both strains, comprising 561 and 604 unigenes in the Chinese and Swiss strains, respectively, followed by translation-pathway, with 309 and 315 unigenes, respectively (Fig. 4). In the Chinese strain, a total of 554 transcription factors were identified including 171 Zf-C2HC-like, 80 ZBTB-like, 65 homeobox-like, and 37 bHLH-like transcription factors (Table S2). Similarly, the Swiss strain contained 557 transcription factors, of which 161were Zf-C2HC-like, 81 ZBTB-like, 68 homeobox-like, and 37 bHLH-like.

Fig. 3.

Fig. 3

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KOG annotations of Trissolcus cultratus predicted proteins. A total of 4041 predicted proteins has a KOG classification among the 26 categories. A represents Chinese strains and B represents Swiss strain.

Fig. 4.

Fig. 4

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KEGG annotation of Trissolcus cultratus predicted proteins. A Cellular Processes, B Environmental Information Processing, C Genetic Information Processing, D Metabolism, E Organismal Systems. a mean Chinese strains and b mean Swiss strain.

All 19,280 and 16,322 unigenes from the Chinese and Swiss strains, respectively, were compared with the protein databases, with priority given to NR and SwissProt. A total of 8,183 and 8,067 CDS were obtained from unigene sequences using BLASTx and translated into amino acid sequences for the Chinese and Swiss strains, respectively (Fig. 5Aa,Ab,Ba,Bb). The transdecoder tool was employed to identify 1,628 and 1,515 single-gene CDS that did not align with the aforementioned protein database for Chinese and Swiss strains, respectively. These sequences were then translated into amino acid sequences by BLASTx and TransDecoder (Fig. 5Ac,Ad,Bc,Bd).

Fig. 5.

Fig. 5

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Coding sequence predictions of Trissolcus cultratus transcriptome by BLASTx and TransDecoder. A mean Chinese strains and B mean Swiss strain. Length distribution of (a) CDS using BLASTx (E-value < 1e−5), (b) proteins using BLASTx, (c) CDS predicted by TransDecoder, and (d) proteins using TransDecoder.

Supplementary information

Supplement tables (31.8KB, xlsx)

Acknowledgements

This study was supported by Yunnan Province Science and Technology Department–Yunnan International Joint Laboratory of Fruit-Vegetable-Flower Invasive Insect Pest Management (Yunnan FVF-PM Joint Lab) (No. 202303AP140018). China’s donation to the CABI Development Fund (VM10051). Francesco Tortorici was supported by the Agritech National Research Center of Italy and received funding from the European Union Next-Generation EU (Piano Nazionale di Ripresa e Resilienza “PNRR”—Missione 4, Componente 2, Investimento 1.4—D.D. 1032 17/06/2022, CN00000022). Tim Haye and Jin-Ping Zhang received core financial support from CABI and its member countries (see http://www.cabi.org/about-cabi/who-we-work-with/keydonors/ accessed on 1st August 2022).

Author contributions

F.Q.L., J.P.Z. and T.H. conceived and designed the experiments. Y.Z.Z., F.T., L.W. and Z.J.S. conducted experiments. F.Q.L., F.T. and S.V.P. analyzed data. All authors contributed to writing and editing of the manuscript.

Data availability

All datasets generated and analyzed during this study have been deposited in public repositories as follows: 1 Raw sequencing reads for both the Chinese and Swiss T. cultratus populations: NCBI Sequence Read Archive (SRA) under BioProject ID PRJNA86304619. Final unigene assembly: NCBI GenBank under accession numbers GLGY0000000020 and GLKP0000000021. 2 Transcriptome unigenes files: Figshare at 10.6084/m9.figshare.2862377322.

Code availability

The following softwares were used for data analysis:

1. Fastp was used for pre-processing for FastQ files. https://github.com/OpenGene/fastp.

2. FastQC was used for quality control. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

3. Trinity 2.6.6 was used to de novo transcriptome assembly. https://github.com/trinityrnaseq/trinityrnaseq.

4. Corset version 4.6 13 was used to enhance the final transcriptome dataset. https://github.com/Oshlack/Corset.

5. BUSCO v5.5.0 were used for assessing assembly quality. https://busco.ezlab.org/.

6. KOBAS-i was used for Gene Ontology (GO) functions and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways analysis. http://bioinfo.org/kobas.

7. Transcription factor identification was conducted using the Animal Transcription Factor Database (version 4.0). https://guolab.wchscu.cn/AnimalTFDB4/#/.

8. TransDecoder (3.0.1) 19 was employed to predict the ORFs. https://github.com/TransDecoder/TransDecoder.

9. OrthorFinder v2.5.5 was used to detect orthologous genes among species. https://github.com/davidemms/OrthoFinder.

10. PosiGene v0.1 was used for adaptive evolution analysis. https://github.com/gengit/PosiGene.

11. Salmon version 1.10.1 was used to quantify transcripts. https://github.com/COMBINE-lab/salmon.

12. DESeq 2 software version 2.11.40.8 was used to conduct differential expression analysis. https://bioconductor.org/packages/release/bioc/html/DESeq2.html.

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/s41597-026-06617-5.

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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:SRP390029 (2025).
  2. Li, F. TSA: Trissolcus cultratus voucher 1 isolate China population, transcriptome shotgun assembly. Genbank.https://identifiers.org/ncbi/insdc:GLGY00000000.1 (2025).

Supplementary Materials

Supplement tables (31.8KB, xlsx)

Data Availability Statement

All datasets generated and analyzed during this study have been deposited in public repositories as follows: 1 Raw sequencing reads for both the Chinese and Swiss T. cultratus populations: NCBI Sequence Read Archive (SRA) under BioProject ID PRJNA86304619. Final unigene assembly: NCBI GenBank under accession numbers GLGY0000000020 and GLKP0000000021. 2 Transcriptome unigenes files: Figshare at 10.6084/m9.figshare.2862377322.

The following softwares were used for data analysis:

1. Fastp was used for pre-processing for FastQ files. https://github.com/OpenGene/fastp.

2. FastQC was used for quality control. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

3. Trinity 2.6.6 was used to de novo transcriptome assembly. https://github.com/trinityrnaseq/trinityrnaseq.

4. Corset version 4.6 13 was used to enhance the final transcriptome dataset. https://github.com/Oshlack/Corset.

5. BUSCO v5.5.0 were used for assessing assembly quality. https://busco.ezlab.org/.

6. KOBAS-i was used for Gene Ontology (GO) functions and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways analysis. http://bioinfo.org/kobas.

7. Transcription factor identification was conducted using the Animal Transcription Factor Database (version 4.0). https://guolab.wchscu.cn/AnimalTFDB4/#/.

8. TransDecoder (3.0.1) 19 was employed to predict the ORFs. https://github.com/TransDecoder/TransDecoder.

9. OrthorFinder v2.5.5 was used to detect orthologous genes among species. https://github.com/davidemms/OrthoFinder.

10. PosiGene v0.1 was used for adaptive evolution analysis. https://github.com/gengit/PosiGene.

11. Salmon version 1.10.1 was used to quantify transcripts. https://github.com/COMBINE-lab/salmon.

12. DESeq 2 software version 2.11.40.8 was used to conduct differential expression analysis. https://bioconductor.org/packages/release/bioc/html/DESeq2.html.

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