Long non-coding RNAs of the trematode Himasthla Elongata (Mehlis, 1831) (Trematoda, Himasthlidae)

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

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.

Full Text

Restricted Access

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

  1. 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)].
  2. 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
  3. 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
  4. 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
  5. Bartel D.P. 2018. Metazoan MicroRNAs. Cell. № 1 (173): 20–51. https://doi.org/10.1016/j.cell.2018.03.006
  6. 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
  7. 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
  8. 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
  9. 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.
  10. 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.
  11. 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
  12. 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
  13. 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
  14. Deininger P. 2011. Alu elements: know the SINEs. Genome Biology; 12 (12): 236. https://doi.org/10.1186/gb-2011-12-12-236
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. 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
  29. 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
  30. 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
  31. 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
  32. 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
  33. Kazazian H.H. 2011. Mobile DNA transposition in somatic cells. BMC Biology: 62. https://doi.org/10.1186/1741-7007-9-62
  34. 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
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. 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
  41. 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
  42. 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
  43. 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
  44. 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
  45. 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
  46. 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
  47. Nefedova L.N., Kim A.I. 2017. Mechanisms of ltr‐retroelement transposition: Lessons from drosophila melanogaster. Viruses: 81. https://doi.org/10.3390/v9040081
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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
  53. 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
  54. 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
  55. 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.
  56. 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
  57. 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
  58. 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
  59. 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
  60. 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
  61. 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
  62. 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
  63. 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
  64. 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
  65. 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
  66. 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
  67. 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
  68. 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
  69. 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
  70. 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
  71. 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
  72. 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
  73. 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
  74. 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.
  75. 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
  76. 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
  77. 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
  78. 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.
  79. 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
  80. 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
  81. 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
  82. Zhang P., 2009. Novel functions for small RNA molecules. Current opinion in molecular therapeutics 6 (11): 641–651. PMC3593927
  83. 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

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure 1. Workflow for lncRNA identification in the H. elongata transcriptome. A – lncRNAs identified based on sequence homology with transposable elements of H. elongata; B – lncRNAs obtained through direct H. elongata transcriptome filtering. ORF – Open reading frame.

Download (1MB)
Indexing metadata
3. Figure 2. The piechart illustrating the percentage of repetitive and unique sequences in the genome of H. elongata.

Download (618KB)
Indexing metadata
4. Figure 3. Piechart representing composition of lncRNAs in the redia-stage transcriptome of H. elongata that share homology with lncRNAs from other trematodes, classified by type: true lncRNAs – 73%, transposable element and viral ORF fragments – 24.7%, and housekeeping gene fragments – 2.3%.

Download (359KB)
Indexing metadata
5. Figure 4. Comparison of two approaches for lncRNA identification in the H. elongata transcriptome: A – direct transcriptome filtering, which primarily identified short lncRNAs; B – еhomology-based search against transposable elements, which predominantly detected longer lncRNAs.

Download (199KB)
Indexing metadata
6. Figure 5. Results of PCR, performed with genomic DNA from rediae (DNA) and cDNA from cercariae (C), metacercariae (M), and rediae (R) as templates, with primers specific to the identified lncRNAs. L – ladder, DNA size marker, b.p. – base pairs, K- – negative control. Primer names corresponding to the selected lncRNAs (see Table 1) are labeled above each lane.

Download (1MB)
Indexing metadata
7. Figure 6. Alignment of nucleotide sequences of PCR products corresponding to putative H. elongata lncRNAs (bottom row) with their respective transcripts (top row) derived from the transcriptome assembly. A–C – are examples of alignments for delnc2.2, delnc1.2 and delnc4.1 amplicons with corresponding transcripts. The colour shows the degree of similarity as determined by the T-Coffe software.

Download (4MB)
Indexing metadata
8. Figure 7. Differential expression of lncRNAs in the trematode H. elongata at the redia, cercaria, and metacercaria stages, based on real-time PCR analysis. Statistical analysis was performed using the Kruskal–Wallis test (for overall group comparisons) and the Mann–Whitney U test (for pairwise comparisons). * p < 0.05. Primer names corresponding to each lncRNA are indicated above the graphs.

Download (927KB)
Indexing metadata

Copyright (c) 2025 Russian Academy of Sciences