Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections

Abstract Background Paratuberculosis (Johne’s disease, JD) is a chronic and enteric disease in a range of ruminants, often caused by Mycobacterium avium subspecies paratuberculosis (MAP) infection, leading to substantial economic losses worldwide. Yet, the molecular underpinning of paratuberculosis...

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Main Authors: Yahui Gao, Jie Cao, Bo Han, Dongxiao Sun
Format: Article
Language:English
Published: BMC 2025-02-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11299-1
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author Yahui Gao
Jie Cao
Bo Han
Dongxiao Sun
author_facet Yahui Gao
Jie Cao
Bo Han
Dongxiao Sun
author_sort Yahui Gao
collection DOAJ
description Abstract Background Paratuberculosis (Johne’s disease, JD) is a chronic and enteric disease in a range of ruminants, often caused by Mycobacterium avium subspecies paratuberculosis (MAP) infection, leading to substantial economic losses worldwide. Yet, the molecular underpinning of paratuberculosis remains elusive. Here we performed RNA sequencing (RNA-seq) and small RNA sequencing (sRNA-seq) of the jejunum tissues from the Holstein cows with three distinct statuses of paratuberculosis, i.e., healthy, subclinical, and clinical to screen potential genes, lncRNAs, and miRNAs associated with the resistance or susceptibility to MAP infection and build ceRNA regulatory networks via miRNAs. Results We applied whole transcriptome sequencing analysis to examine the jejunum tissue in nine Holstein cows. Starting with 19,994 expressed genes, 13,529 lncRNAs, and 735 miRNAs, we screened out differentially expressed genes (DEGs), lncRNAs, and miRNAs of three comparison groups, i.e., clinical vs. healthy, subclinical vs. healthy, and clinical vs. subclinical, subsequently identifying ceRNA pairs. Ultimately, we detected 76, 74, and 24 DEGs, 19, 39, and 10 lncRNAs, as well as 28, 61, and 20 miRNAs across the three comparison groups, respectively. Through integrating these DEGs with functional annotation, previously reported QTLs, and GWAS results, we proposed eight genes (LYZ, LYZ1, BOLA-DQB, BOLA-DQA1, TAP, CATD, VNN1, and PPARG), six lncRNAs, 48 miRNAs, and 107 ceRNA pairs implying their potential associations with susceptibility to MAP infection. Conclusion The present study provided a global view of the dynamics in transcriptomes of the bovine jejunum tissues in terms of JD status. Our results demonstrated that not only mRNAs but also lncRNAs and miRNAs played important roles in regulating MAP infection in dairy cattle. This study provided a valuable resource for understanding the molecular basis of JD, potentially contributing to the genetic improvement of JD resistance in dairy cattle.
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spelling doaj-art-239c28b8b0574213bfe23955cd178d2c2025-02-09T12:13:47ZengBMCBMC Genomics1471-21642025-02-0126112110.1186/s12864-025-11299-1Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infectionsYahui Gao0Jie Cao1Bo Han2Dongxiao Sun3Key Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory of Animal Breeding, College of Animal Science and Technology, China Agricultural UniversityCollege of Veterinary Medicine, China Agricultural UniversityKey Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory of Animal Breeding, College of Animal Science and Technology, China Agricultural UniversityKey Laboratory of Animal Genetics and Breeding of Ministry of Agriculture, National Engineering Laboratory of Animal Breeding, College of Animal Science and Technology, China Agricultural UniversityAbstract Background Paratuberculosis (Johne’s disease, JD) is a chronic and enteric disease in a range of ruminants, often caused by Mycobacterium avium subspecies paratuberculosis (MAP) infection, leading to substantial economic losses worldwide. Yet, the molecular underpinning of paratuberculosis remains elusive. Here we performed RNA sequencing (RNA-seq) and small RNA sequencing (sRNA-seq) of the jejunum tissues from the Holstein cows with three distinct statuses of paratuberculosis, i.e., healthy, subclinical, and clinical to screen potential genes, lncRNAs, and miRNAs associated with the resistance or susceptibility to MAP infection and build ceRNA regulatory networks via miRNAs. Results We applied whole transcriptome sequencing analysis to examine the jejunum tissue in nine Holstein cows. Starting with 19,994 expressed genes, 13,529 lncRNAs, and 735 miRNAs, we screened out differentially expressed genes (DEGs), lncRNAs, and miRNAs of three comparison groups, i.e., clinical vs. healthy, subclinical vs. healthy, and clinical vs. subclinical, subsequently identifying ceRNA pairs. Ultimately, we detected 76, 74, and 24 DEGs, 19, 39, and 10 lncRNAs, as well as 28, 61, and 20 miRNAs across the three comparison groups, respectively. Through integrating these DEGs with functional annotation, previously reported QTLs, and GWAS results, we proposed eight genes (LYZ, LYZ1, BOLA-DQB, BOLA-DQA1, TAP, CATD, VNN1, and PPARG), six lncRNAs, 48 miRNAs, and 107 ceRNA pairs implying their potential associations with susceptibility to MAP infection. Conclusion The present study provided a global view of the dynamics in transcriptomes of the bovine jejunum tissues in terms of JD status. Our results demonstrated that not only mRNAs but also lncRNAs and miRNAs played important roles in regulating MAP infection in dairy cattle. This study provided a valuable resource for understanding the molecular basis of JD, potentially contributing to the genetic improvement of JD resistance in dairy cattle.https://doi.org/10.1186/s12864-025-11299-1ParatuberculosisRNA-seqsRNA-seqHolstein cattle
spellingShingle Yahui Gao
Jie Cao
Bo Han
Dongxiao Sun
Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
BMC Genomics
Paratuberculosis
RNA-seq
sRNA-seq
Holstein cattle
title Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
title_full Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
title_fullStr Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
title_full_unstemmed Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
title_short Preliminary exploration of mRNA, lncRNA, and miRNA expressions in the bovine jejunum unveils novel aspects of Mycobacterium avium subspecies paratuberculosis infections
title_sort preliminary exploration of mrna lncrna and mirna expressions in the bovine jejunum unveils novel aspects of mycobacterium avium subspecies paratuberculosis infections
topic Paratuberculosis
RNA-seq
sRNA-seq
Holstein cattle
url https://doi.org/10.1186/s12864-025-11299-1
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