Long non-coding RNAs of the trematode Himasthla Elongata (Mehlis, 1831) (Trematoda, Himasthlidae)
- Authors: Smolyaninova A.R.1, Gabdrakhmanova M.S.1, Romanovich A.E.2, Efeykin B.D.3, Solovyeva A.I.1,4
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Affiliations:
- Институт цитологии РАН
- Санкт-Петербургский государственный университет
- Институт проблем экологии и эволюции имени А.Н. Северцова РАН
- Зоологический институт РАН
- Issue: Vol 59, No 3 (2025)
- Pages: 231-251
- Section: Articles
- URL: https://rjsvd.com/0031-1847/article/view/687156
- DOI: https://doi.org/10.31857/S0031184725030044
- EDN: https://elibrary.ru/SXEHLX
- ID: 687156
Cite item
Abstract
The molecular mechanisms regulating the life cycle of trematodes remain largely unexplored to date. It is hypothesized that the non-coding portion of the genome, particularly long non-coding RNAs (lncRNAs) and repetitive elements, plays a key role in this regulation. In this study, we present the first identification of lncRNAs in the trematode Himasthla elongata based on transcriptome analysis combined with repeat homology assessment. Approximately half of the identified lncRNAs contain transposon-derived regions, reflecting the fact that transposable elements occupy 57.5% of the genome. The expression of several lncRNAs was confirmed across the redia, cercaria, and metacercaria life stages. These findings provide a basis for further study of the role of mobile elements in the formation of regulatory RNAs and in the evolution of transcription regulation mechanisms in trematodes.
Keywords
Full Text

About the authors
A. R. Smolyaninova
Институт цитологии РАН
Email: orcinuca@gmail.com
Russian Federation, Тихорецкий пр., 4, Санкт-Петербург, 194064
M. S. Gabdrakhmanova
Институт цитологии РАН
Email: orcinuca@gmail.com
Russian Federation, Тихорецкий пр., 4, Санкт-Петербург, 194064
A. E. Romanovich
Санкт-Петербургский государственный университет
Email: orcinuca@gmail.com
Russian Federation, Университетская наб. 7/9, Санкт-Петербург, 199034
B. D. Efeykin
Институт проблем экологии и эволюции имени А.Н. Северцова РАН
Email: orcinuca@gmail.com
Russian Federation, Ленинский пр-т, 33, Москва, 119071
A. I. Solovyeva
Институт цитологии РАН; Зоологический институт РАН
Author for correspondence.
Email: orcinuca@gmail.com
Russian Federation, Тихорецкий пр., 4, Санкт-Петербург, 194064; Университетская наб. 1, Санкт-Петербург, 199034
References
- Макарова Ю.А., Крамеров Д.А. 2007. Некодирующие РНК. Биохимия 1427–1448. [Makarova Y.A., Kramerov D.A. 2007. Non-coding RNA. Biochemistry 1427–1448. (in Russian)].
- Anderson L., Amara, M.S., Beckedorff F., Silva L.F., Guigas P.V., Pires D.S. et al. 2018. Schistosoma mansoni: A comprehensive analysis of long non-coding RNAs reveals novel regulators of infection, development and sexual differentiation. PLoS Neglected Tropical Diseases 12 (2): e0006265. https://doi.org/10.1371/journal.ppat.1011369
- Arkhipova I.R., 2018. Neutral theory, transposable elements, and eukaryotic genome evolution. Molecular Biology and Evolution 35: 1332–1337. https://doi.org/10.1093/molbev/msy083
- Baril T., Pym A., Bass C., Hayward A. 2023. Transposon accumulation at xenobiotic gene family loci in aphids. Genome Res 33: 1718–1733. https://doi.org/10.1101/gr.277820.123
- Bartel D.P. 2018. Metazoan MicroRNAs. Cell. № 1 (173): 20–51. https://doi.org/10.1016/j.cell.2018.03.006
- Bolger A.M., Lohse M., Usadel B. 2014. Trimmomatic: A flexible trimmer for Illumina Sequence Data. Bioinformatics 30 (15): 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
- Bourque G., Burns K.H., Gehring M., Gorbunova V., Seluanov A., Hammell M., Imbeault M., Izsvák Z., Levin H.L., Macfarlan T.S., Mager D.L., Feschotte C. 2018. Ten things you should know about transposable elements 06 Biological Sciences 0604 Genetics. Genome Biology 19: 199. https://doi.org/10.1186/s13059-018-1577-z
- Buddenborg S.K., Lu Z., Sankaranarayan G., Doyle S.R., Berriman M. 2023. The stage- and sex-specific transcriptome of the human parasite Schistosoma mansoni. Sci Data 10: 775. https://doi.org/10.1038/s41597-023-02674-2
- Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55 (4): 611–622. https://doi.org/10.1373/clinchem.2008.112797.
- Chen S., Zhou Y., Chen Y., Gu J. 2018. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34 (17): i884-i890. https://doi.org/10.1093/bioinformatics/bty560.
- Cock P.J., Chilton J.M., Grüning B., Johnson J.E., Soranzo N. 2015. NCBI BLAST+ integrated into Galaxy. GigaScience 1 (4): s13742–015–0080–7. https://doi.org/10.1186/s13742-015-0080-7
- Copeland C.S., Mann V.H., Morales M.E., Kalinna B.H., Brindley P.J. 2005. The Sinbad retrotransposon from the genome of the human blood fluke, Schistosoma mansoni, and the distribution of related Pao-like elements. BMC Ecology and Evolution 5: 20. https://doi.org/10.1186/1471-2148-5-20
- Dang-Nguyen T.Q., Torres-Padilla M.E. 2015. How cells build totipotency and pluripotency: Nuclear, chromatin and transcriptional architecture. Current Opinion in Cell Biology 9–15. https://doi.org/10.1016/j.ceb.2015.04.006
- Deininger P. 2011. Alu elements: know the SINEs. Genome Biology; 12 (12): 236. https://doi.org/10.1186/gb-2011-12-12-236
- DeMarco R., Venancio T.M., Verjovski-Almeida S. 2006. SmTRC1, a novel Schistosoma mansoni DNA transposon, discloses new families of animal and fungi transposons belonging to the CACTA superfamily. Ecology and Evolution 6: 89. https://doi.org/10.1186/1471-2148-6-89
- Derrien T., Johnson R., Bussotti G., Tanzer A., Djebali S., Tilgner H., Guernec G., Martin D., Merkel A., Knowles D.G., Lagarde J., Veeravalli L., Ruan X., Ruan Y., Lassmann T., Carninci P., Brown J.B., Lipovich L., Gonzalez J.M., Thomas M., Davis C.A., Shiekhattar R., Gingeras T.R., Hubbard T.J., Notredame C., Harrow J., Guigó R. 2012. The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Research 22 (9): 1775–1789. https://doi.org/10.1101/gr.132159.111
- DeVeale B., Swindlehurst-Chan J., Blelloch R. 2021. The roles of microRNAs in mouse development. Nature Reviews Genetics: 307–323. https://doi.org/10.1038/s41576-020-00309-5
- Djebali S., Davis C.A., Merkel A., Dobin A., Lassmann T., Mortazavi A., Tanzer A. et al. 2012. Landscape of transcription in human cells. Nature 489: 101–108. https://doi.org/10.1038/nature11233
- Drew A.C., Brindley P.J. 1997. A retrotransposon of the non-long terminal repeat class from the human blood fluke Schistosoma mansoni. Similarities to the chicken-repeat-1-like elements of vertebrates. Mol. Bio.l Evol. 14(6): 602–610. https://doi.org/10.1093/oxfordjournals.molbev.a025799
- Fort V., Khelifi G., Hussein S.M.I. 2021. Long non-coding RNAs and transposable elements: A functional relationship. Biochimica et Biophysica Acta (BBA) – Molecular Cell Research: 118837. https://doi.org/10.1016/j.bbamcr.2020.118837
- Fromm B., Ovchinnikov V., Høye E., Bernal D., Hackenberg M., Marcilla A. 2017. On the presence and relative abundance of microRNAs in different tissues of the liver fluke Fasciola hepatica. International Journal for Parasitology 47 (11): 695–702. https://doi.org/10.1016/j.ijpara.2015.06.002
- Gil N., Ulitsky I. 2020. Regulation of gene expression by cis-acting long non-coding RNAs. Nat. Rev. Genet. 21(2): 102–117. https://doi.org/10.1038/s41576-019-0184-5
- Gogvadze E., Buzdin A. 2009. Retroelements and their impact on genome evolution and functioning. Cellular and Molecular Life Sciences: 3727–3742. https://doi.org/10.1007/s00018-009-0107-2
- Gurevich A., Saveliev V., Vyahhi N., Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 29 (8): 1072–1075. https://doi.org/10.1093/bioinformatics/btt086
- Haas B.J., Papanicolaou A., Yassour M., Grabherr M., Blood P.D. et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8 (8): 1494–1512. https://doi.org/10.1038/nprot.2013.084
- Hadjiargyrou M., Delihas N. 2013. The intertwining of transposable elements and non-coding RNAs. International Journal of Molecular Sciences: 13307–13328. https://doi.org/10.3390/ijms140713307
- Hammond S.M. 2015. An overview of microRNAs. Adv Drug Deliv Rev. 87:3-14. https://doi.org/10.1016/j.addr.2015.05.001
- Han S., Liang Y., Ma Q., Xu Y., Zhang Y., Du W., Wang C., Li Y. 2019. LncFinder: an integrated platform for long non-coding RNA identification utilizing sequence intrinsic composition, structural information and physicochemical property. Briefings in Bioinformatics 6 (20): 2009–2027. https://doi.org/10.1093/bib/bby065
- Houhou H., Puckelwaldt O., Strube C., Haeberlein S. 2019. Reference gene analysis and its use for kinase expression profiling in Fasciola hepatica. Scientific Reports:15867. https://doi.org/10.1038/s41598-019-52416-x
- Johnson R., Guigó R. 2014. The RIDL hypothesis: Transposable elements as functional domains of long noncoding RNAs: 20. https://doi.org/10.1261/rna.044560.114
- Kalendar R., Muterko A., Boronnikova S. 2021. Retrotransposable Elements: DNA Fingerprinting and the Assessment of Genetic Diversity, in: Methods in Molecular Biology: 959-976. https://doi.org/10.1007/978-1-0716-0997-2_15
- Kapusta A., Feschotte C. 2014. Volatile evolution of long noncoding RNA repertoires: Mechanisms and biological implications. Trends in Genetics: 439–452. https://doi.org/10.1016/j.tig.2014.08.004
- Kazazian H.H. 2011. Mobile DNA transposition in somatic cells. BMC Biology: 62. https://doi.org/10.1186/1741-7007-9-62
- Kelley D., Rinn J. 2012. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol 13: 107. https://doi.org/10.1186/gb-2012-13-11-r107
- Kim H.C., Khalil A.M., Jolly E.R. 2020. LncRNAs in molluscan and mammalian stages of parasitic schistosomes are developmentally-regulated and coordinately expressed with protein-coding genes. RNA Biology 17: 805-815. https://doi.org/10.1080/15476286.2020.1729594
- Kim S.H., Kong Y., Bae Y.A. 2017. Recurrent emergence of structural variants of LTR retrotransposon CsRn1 evolving novel expression strategy and their selective expansion in a carcinogenic liver fluke, Clonorchis sinensis. Molecular and Biochemical Parasitology 214: 14–26. https://doi.org/10.1016/j.molbiopara.2017.03.004
- Kumar S., Stecher G., Suleski M., Sanderford M., Sharma S., Tamura K. 2024. MEGA12: Molecular Evolutionary Genetic Analysis version 12 for adaptive and green computing. Molecular Biology and Evolution12 (41): msae263. https://doi.org/10.1093/molbev/msae263
- Laha T., Kaewkrai N., Loukas A., Brindley P.J. 2005. Characterization of SR3 reveals abundance of non-LTR retrotransposons of the RTE clade in the genome of the human blood fluke, Schistosoma mansoni. BMC Genomics 6: 154. https://doi.org/10.1186/1471-2164-6-154
- Laha T., Loukas A., Smyth D.J., Copeland C.S., Brindley P.J. 2005. Erratum: The fugitive LTR retrotransposon from the genome of the human blood fluke, Schistosoma mansoni. International Journal for Parasitology (2004): 1365–1375. https://doi.org/10.1016/j.ijpara.2005.02.001
- Li F., Zhang Y., Li C., Li F., Gan B., Yu H., Li J., Feng X., Hu W. 2024. Clonorchis sinensis infection induces pathological changes in feline bile duct epithelium and alters biliary microbiota composition. Parasite 31–53. https://doi.org/10.1051/parasite/2024053
- Lower S.E., Dion-Côté A.M., Clark A.G., Barbash D.A. 2019. Special issue: Repetitive DNA sequences. Genes (Basel): 896. https://doi.org/10.3390/genes10110896
- Luo X., Cui, K., Wang Z., Li Z., Wu Z., Huang W., Zhu X.Q., Ruan J., Zhang W., Liu Q. 2021. High-quality reference genome of Fasciola gigantica: Insights into the genomic signatures of transposon-mediated evolution and specific parasitic adaption in tropical regions. PLoS Negl Trop Dis 15: e0009750. https://doi.org/10.1371/JOURNAL.PNTD.0009750
- Maciel L.F., Morales-Vicente D.A., Verjovski-Almeida S. 2020. Dynamic expression of long non-coding rnas throughout parasite sexual and neural maturation in Schistosoma japonicum. Non-coding RNA 6: 15. https://doi.org/10.3390/ncrna6020015
- Márton É., Varga A., Domoszlai D., Buglyó G., Balázs A., Penyige A., Balogh I., Nagy B., Szilágyi M. 2025. Non-Coding RNAs in Cancer: Structure, Function, and Clinical Application. Cancers (Basel) 8; 17(4): 579. https://doi.org/10.3390/cancers17040579
- McNulty S.N., Tort J.F., Rinaldi G., Fischer K., Rosa B.A., Smircich P. et al. 2017. Genomes of Fasciola hepatica from the Americas reveal colonization with Neorickettsia endobacteria related to the agents of potomac horse and human sennetsu fevers. PLoS Genetics 13: e1006537. https://doi.org/10.1371/journal.pgen.1006537
- McVeigh P., McCammick E., Robb E., Brophy P., Morphew R.M., Marks N.J., Maule A.G. 2023. Discovery of long non-coding RNAs in the liver fluke, Fasciola hepatica. PLoS Neglected Tropical Diseases 17: e0011663. https://doi.org/10.1371/journal.pgen.1006537
- Nefedova L.N., Kim A.I. 2017. Mechanisms of ltr‐retroelement transposition: Lessons from drosophila melanogaster. Viruses: 81. https://doi.org/10.3390/v9040081
- Nesterenko M.A., Starunov V.V., Shchenkov S.V., Maslova A.R., Denisova S.A., Granovich A.I., Dobrovolskij A.A., Khalturin K.V. 2020. Molecular signatures of the rediae, cercariae and adult stages in the complex life cycles of parasitic flatworms (Digenea: Psilostomatidae). Parasites and Vectors. BioMed Central Ltd. 13 (1): 559. https://doi.org/10.1186/s13071-020-04424-4
- Nesterenko M., Shchenkov S., Denisova S., Starunov V. 2022. The digenean complex life cycle: phylostratigraphy analysis of the molecular signatures. Biological Communications 67 (2): 65–87. https://doi.org/10.21638/spbu03.2022.201
- Nolan T., Hands R.E., Bustin S.A. 2006. Quantification of mRNA using real-time RT-PCR. Nature Protocols 1 (3): 1559–1582. https://doi.org/10.1038/nprot.2006.236
- Notredame C., Higgins D.G., Heringa J. 2000. T-Coffee: A novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 205–217. https://doi.org/10.1006/jmbi.2000.4042
- Palazzo A.F., Lee E.S. 2015. Non-coding RNA: what is functional and what is junk? Frontiers in Genetics 6: 2. https://doi.org/10.3389/fgene.2015.00002
- Philippsen G.S. 2021. Transposable elements in the genome of human parasite Schistosoma mansoni: A review. Tropical Medicine and Infectious Disease: 126. https://doi.org/10.3390/tropicalmed6030126
- Prjibelski A., Antipov D., Meleshko D., Lapidus A., Korobeynikov A. 2020. Using SPAdes de novo assembler. Current Protocols in Bioinformatics 70, e102. https://doi.org/10.1002/cpbi.102
- Ramakrishnaiah Y., Kuhlmann L., Tyagi S. 2020. Towards a comprehensive pipeline to identify and functionally annotate long noncoding RNA (lncRNA). Computers in Biology and Medicine 127: 104028. https://doi.org/10.1016/j.compbiomed.2020.104028.
- Richard G.-F., Kerrest A., Dujon B. 2008. Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes. Microbiology and Molecular Biology Reviews 72. https://doi.org/10.1128/mmbr.00011-08
- Rodriguez M., Makałowski W. 2022. Software evaluation for de novo detection of transposons. Mobile DNA: 14. https://doi.org/10.1186/s13100-022-00266-2
- Rosa B.A., Choi Y.J., McNulty S.N., Jung H., Martin J., Agatsuma T., Sugiyama H., Le T.H., Doanh P.N., Maleewong W., Blair D., Brindley P.J., Fischer P.U., Mitreva M. 2020. Comparative genomics and transcriptomics of 4 Paragonimus species provide insights into lung fluke parasitism and pathogenesis: giaa073. https://doi.org/10.1093/GIGASCIENCE/GIAA073
- Scarpa A., Kofler R. 2023. The impact of paramutations on the invasion dynamics of transposable elements. Genetics 225: 181. https://doi.org/10.1093/genetics/iyad181
- Schmittgen T.D., Livak K.J. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. https://doi.org/10.1006/meth.2001.1262
- Simão F.A., Waterhouse R.M., Ioannidis P., Kriventseva E.V., Zdobnov E.M. 2015. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31 (19): 3210–3212. https://doi.org/10.1093/bioinformatics/btv351
- Sirekbasan S., Gurkok Tan T. 2021. In Silico Analysis of Common Long Noncoding RNAs in Schistosoma mansoni and Schistosoma haematobium. Journal of Tropical Medicine 1–8. https://doi.org/10.1155/2021/6617118
- Skalon E.K., Panyushev N.V., Podgornaya O.I., Smolyaninova A.R., Solovyeva A.I. 2024. Expression of transposable elements throughout the Fasciola hepatica trematode life cycle. Non-Coding RNA 4 (10): 39. https://doi.org/10.3390/ncrna10040039
- Smith M., Yadav S., Fagunloye O.G., Pels N.A., Horton D.A., Alsultan N., Borns A., Cousin C., Dixon F., Mann V.H., Lee C., Brindley P.J., El-Sayed N.M., Bridger J.M., Knight M. 2021. Piwi silencing mechanism involving the retrotransposon nimbus orchestrates resistance to infection with Schistosoma mansoni in the snail vector, Biomphalaria glabrata. PLoS Neglected Tropical Disease 15: e0009094. https://doi.org/10.1371/journal.pntd.0009094
- Solovyeva A., Levakin I., Zorin E., Adonin L., Khotimchenko Y., Podgornaya O. 2021. Transposons-based clonal diversity in trematode involves parts of cr1 (Line) in eu-and heterochromatin. Genes (Basel) 12: 1129. https://doi.org/10.3390/genes12081129
- Song N., Wang Y., Gu X.D., Chen Z.Y., Shi L. 2013. Effect of siRNA-mediated knockdown of eIF3c gene on survival of colon cancer cells. Journal of Zhejiang University-SCIENCE B 14: 451–459. https://doi.org/10.1631/jzus.B1200230
- Statello L., Guo C.-J., Chen L.-L., Huarte M. 2020. Gene regulation by long non-coding RNAs and its biological functions. Nature Reviews Molecular Cell Biology 22: 96–118. https://doi.org/10.1038/s41580-020-00315-9
- Ulitsky I., Bartel D.P. 2013. lncRNAs: Genomics, evolution, and mechanisms. Cell 154 (1): 26–46. https://doi.org/10.1016/j.cell.2013.06.020
- Venancio T.M., Wilson R.A., Verjovski-Almeida S., DeMarco R. 2010. Bursts of transposition from non-long terminal repeat retrotransposon families of the RTE clade in Schistosoma mansoni. Int. J. Parasitol. 40(6): 743–749. https://doi.org/10.1016/j.ijpara.2009.11.013
- Villar D., Flicek P., Odom D.T. 2014. Evolution of transcription factor binding in metazoans-mechanisms and functional implications. Nature Reviews Genetics 221–233. https://doi.org/10.1038/nrg3481
- Wang J., Yu Y., Shen H., Qing T., Zheng Y., Li Q., Mo X., Wang S., L, N., Chai R., Wu X. 2017. Dynamic transcriptomes identify biogenic pathways during the larval development of Schistosoma japonicum. PLOS Neglected Tropical Diseases 11 (9): e0006460. https://doi.org/10.1038/ncomms14693
- Wang S.S., Chen D., He J.J., Zheng W. Bin, Tian A.L., Zhao G.H., Elsheikha H.M., Zhu X.Q. 2021. Fasciola gigantica – derived excretory-secretory products alter the expression of mRNAs, miRNAs, lncRNAs, and circRNAs involved in the immune response and metabolism in goat peripheral blood mononuclear cells. Frontiers in Immunology: 12. https://doi.org/10.3389/fimmu.2021.653755
- Werding B. 1969. Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Marine Biology 3: 306–333. https://doi.org/10.1007/BF00698861
- Wheeler T.J., Clements J., Eddy S.R., Hubley R., Jones T.A., Jurka J., Smit A.F., Finn R.D. 2013. Dfam: a database of repetitive DNA based on profile hidden Markov models. Nucleic Acids Research: 70–82. https://doi.org/10.1093/nar/gks1265.
- Wicker T., Sabot F., Hua-Van A., Bennetzen J.L., Capy P., Chalhoub B., Flavell A., Leroy P., Morgante M., Panaud O., Paux E., Sanmiguel P., Schulman A.H. 2007. A unified classification system for eukaryotic transposable elements: 306–333. https://doi.org/10.1038/nrg2165
- Wood D.E., Lu J., Langmead B. 2019. Improved metagenomic analysis with Kraken 2. Genome Biology 20 (1): 257. https://doi.org/10.1186/s13059-019-1891-0
- Wu Z., Liu X., Liu L., Deng H., Zhang J., Xu Q., Cen B., Ji A. 2014. Regulation of lncRNA expression. Cellular et Molecular Biology Letters 19: 561–575. https://doi.org/10.2478/s11658-014-0212-6
- Wucher V., Legeai F., Hédan B., Rizk G., Lagoutte L., Leeb T. et al. 2017. FEELnc: a tool for long non-coding RNA annotation and its application to the dog transcriptome. Nucleic Acids Research 45 (8): e57. https://doi.org/10.1093/nar/gkw1306.
- Young N.D., Nagarajan N., Lin S.J., Korhonen P.K., Jex A.R et al. 2014. The Opisthorchis viverrini genome provides insights into life in the bile duct. Nature Communications 5: 222–231. https://doi.org/10.1038/ncomms5378
- Yushkova E., Moskalev A. 2023. Transposable elements and their role in aging. Ageing Research Reviews: 101881. https://doi.org/10.1016/j.arr.2023.101881
- Zhang J., Wu L., Wang C., Xie X., Han Y. 2024. Research Progress of Long Non-Coding RNA in Tumor Drug Resistance: A New Paradigm. Drug Des Devel Ther. 18: 1385–1398. https://doi.org/10.2147/DDDT.S448707
- Zhang P., 2009. Novel functions for small RNA molecules. Current opinion in molecular therapeutics 6 (11): 641–651. PMC3593927
- Zhou Y., Zheng H., Chen Y., Zhang L., Wang K., Guo J., et al. 2009. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460: 641–651. https://doi.org/10.1038/nature08140
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