Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus

Abstract The intestine of Haemonchus contortus is an essential tissue that has been indicated to be a major target for the prevention of haemonchosis caused by this parasitic nematode of small ruminants. Biological peculiarities of the intestine warrant in-depth exploitation, which can be leveraged...

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Main Authors: Caixian Zhou, Waresi Tuersong, Lu Liu, Wenda Di, Li He, Fangfang Li, Chunqun Wang, Min Hu
Format: Article
Language:English
Published: BMC 2024-01-01
Series:Veterinary Research
Subjects:
Online Access:https://doi.org/10.1186/s13567-023-01254-x
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author Caixian Zhou
Waresi Tuersong
Lu Liu
Wenda Di
Li He
Fangfang Li
Chunqun Wang
Min Hu
author_facet Caixian Zhou
Waresi Tuersong
Lu Liu
Wenda Di
Li He
Fangfang Li
Chunqun Wang
Min Hu
author_sort Caixian Zhou
collection DOAJ
description Abstract The intestine of Haemonchus contortus is an essential tissue that has been indicated to be a major target for the prevention of haemonchosis caused by this parasitic nematode of small ruminants. Biological peculiarities of the intestine warrant in-depth exploitation, which can be leveraged for future disease control efforts. Here, we determined the intestinal ncRNA (lncRNA, circRNA and miRNA) atlas using whole-transcriptome sequencing and bioinformatics approaches. In total, 4846 novel lncRNA, 982 circRNA, 96 miRNA (65 known and 31 novel) and 8821 mRNA were identified from the H. contortus intestine. The features of lncRNA, circRNA and miRNA were fully characterized. Comparison of miRNA from the intestines and extracellular vesicles supported the speculation that the miRNA from the latter were of intestinal origin in H. contortus. Further function analysis suggests that the cis-lncRNA targeted genes were involved in protein binding, intracellular anatomical structure, organelle and cellular process, whereas the circRNA parental genes were mainly enriched in molecular function categories, such as ribonucleotide binding, nucleotide binding, ATP binding and carbohydrate derivative binding. The miRNA target genes were related to the cellular process, cellular response to stimulus, cellular protein modification process and signal transduction. Moreover, competing endogenous RNA network analysis revealed that the majority of lncRNA, circRNA and mRNA only have one or two binding sites with specific miRNA. Lastly, randomly selected circRNA, lncRNA and miRNA were verified successfully using RT-PCR. Collectively, these data provide the most comprehensive compilation of intestinal transcripts and their functions, and it will be helpful to decipher the biological and molecular complexity of the intestine and lay the foundation for further functional research.
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spelling doaj.art-e7b64dd6fb94405f90641ca099992e4e2024-01-07T12:39:42ZengBMCVeterinary Research1297-97162024-01-0155111510.1186/s13567-023-01254-xNon-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortusCaixian Zhou0Waresi Tuersong1Lu Liu2Wenda Di3Li He4Fangfang Li5Chunqun Wang6Min Hu7State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityCollege of Veterinary Medicine, Xinjiang Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityCollege of Animal Science and Technology, Guangxi UniversitySchool of Basic Medical Sciences, Hubei University of MedicineCollege of Biology and Food Engineering, Chongqing Three Gorges UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityAbstract The intestine of Haemonchus contortus is an essential tissue that has been indicated to be a major target for the prevention of haemonchosis caused by this parasitic nematode of small ruminants. Biological peculiarities of the intestine warrant in-depth exploitation, which can be leveraged for future disease control efforts. Here, we determined the intestinal ncRNA (lncRNA, circRNA and miRNA) atlas using whole-transcriptome sequencing and bioinformatics approaches. In total, 4846 novel lncRNA, 982 circRNA, 96 miRNA (65 known and 31 novel) and 8821 mRNA were identified from the H. contortus intestine. The features of lncRNA, circRNA and miRNA were fully characterized. Comparison of miRNA from the intestines and extracellular vesicles supported the speculation that the miRNA from the latter were of intestinal origin in H. contortus. Further function analysis suggests that the cis-lncRNA targeted genes were involved in protein binding, intracellular anatomical structure, organelle and cellular process, whereas the circRNA parental genes were mainly enriched in molecular function categories, such as ribonucleotide binding, nucleotide binding, ATP binding and carbohydrate derivative binding. The miRNA target genes were related to the cellular process, cellular response to stimulus, cellular protein modification process and signal transduction. Moreover, competing endogenous RNA network analysis revealed that the majority of lncRNA, circRNA and mRNA only have one or two binding sites with specific miRNA. Lastly, randomly selected circRNA, lncRNA and miRNA were verified successfully using RT-PCR. Collectively, these data provide the most comprehensive compilation of intestinal transcripts and their functions, and it will be helpful to decipher the biological and molecular complexity of the intestine and lay the foundation for further functional research.https://doi.org/10.1186/s13567-023-01254-xHaemonchus contortusintestinelong non-coding RNAcircRNAmiRNAceRNA
spellingShingle Caixian Zhou
Waresi Tuersong
Lu Liu
Wenda Di
Li He
Fangfang Li
Chunqun Wang
Min Hu
Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
Veterinary Research
Haemonchus contortus
intestine
long non-coding RNA
circRNA
miRNA
ceRNA
title Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
title_full Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
title_fullStr Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
title_full_unstemmed Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
title_short Non-coding RNA in the gut of the blood-feeding parasitic worm, Haemonchus contortus
title_sort non coding rna in the gut of the blood feeding parasitic worm haemonchus contortus
topic Haemonchus contortus
intestine
long non-coding RNA
circRNA
miRNA
ceRNA
url https://doi.org/10.1186/s13567-023-01254-x
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