- Chicken cecal DNA methylome alteration in the response to Salmonella enterica serovar Enteritidis inoculation. - DNA methylation is involved in regulatory processes including gene expression, chromatin structure and genomic imprinting. - To understand the methylation regulation in the response to SE inoculation in chicken, the genome-wide DNA methylation profile following SE inoculation was analyzed through whole-genome bisulfite sequencing in the current study.. - Results: There were clean reads and unique reads in the control group, and clean reads and unique reads in the inoculated group. - The methylation density in the gene body was higher than that in the upstream and downstream regions of the gene. - Conclusions: The genome-wide DNA methylation profile in the response to SE inoculation in chicken was analyzed. - SE inoculation promoted the DNA methylation in the chicken cecum and caused methylation alteration in immune- and metabolic- related genes. - Wnt signal pathway, miRNAs and HOX gene family may play crucial roles in the methylation regulation of SE inoculation in chicken. - The findings herein will deepen the understanding of epigenetic regulation in the response to SE inoculation in chicken.. - The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. - If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. - It is estimated that Salmonella enteritidis causes 1.3 million cases of gastroenteritis, and more than 350 died each year in the United States [7].. - DNA methylation, one of the major epigenetic modifi- cations, is involved in the regulatory processes including gene expression, chromatin structure, genomic imprint- ing, transposon silencing, X-chromosome inactivation, disease response and individual development [9–11].. - DNA methylation in gene body interferes with transcript elongation [12–14], and DNA methylation of the first exon is tightly linked to transcriptional silencing [15, 16]. - DNA methylation has been reported in many species such as human [26], bovine [21], soybean [27], rat [28], rice [29]. - Aberrant DNA methylation is associ- ated with several immune deficiencies and autoimmune disorders in human [31]. - The potential role of DNA methylation in regulating disease resistance in chickens has been reported through analyzing genes within the differentially methylated regions (DMR) between Fayoumi and Leghorn chicken [25]. - Functional DNA methylated loci play important roles in regulating ex- pression of genes involved in the inflammatory response and tissue injury after Avian pathogenic Escherichia coli infection in chicken [32]. - The TLR4 methylation is related to expression of genes involved in the MyD88 signaling pathway in S. - While, genome-wide DNA methylation variation of chickens infected with Salmon- ella is not fully clarified.. - The aim of the current study was to in- vestigate the global DNA methylation profiles in the chicken cecum and to identify potentially functional methylated regions and genes related to host response to SE inoculation through WGBS.. - Analysis of genome-wide DNA methylation data. - (mCHH/CHH) and 1.00% (mCHG/CHG) identified in the control group. - (mCHG/CHG) were identified in the inoculated group.. - CAH and CHT were preferred in the mCHH type (Fig. - DNA methylation in different gene regions. - To better understand methylation pattern in the genome, the methylation in different gene regions was analyzed (Fig. - The level of DNA methylation in the first exon was the lowest across all exons, but higher than that in introns. - In general, the methylation density in gene body was higher than that in the upstream and downstream of the gene.. - There were 457 miRNAs in the top 1000 genes with higher DMC density, 324 miRNAs in the top 500 genes.. - There were 82.5% DMR located in the distal intergenic region, only 0.02% in the 1st intron (Fig. - There were 8946 differentially methylated genes identified, including 3639 hypo-methylated genes and 5307 hyper-methylated genes in the inoculated group compared with the control group. - There were more than 1000 differentially meth- ylated genes in Chr differentially methylated genes in Chr2, 3, 4 and differentially methyl- ated genes in the Chr6 – 28 excluding Chr16, 22, 24 and differentially methylated genes in Chr and Z. - In term of the CC, the DMGs were mainly located in the extracellular region, cell, nucleoid, organelle part, virion part and membrane part. - CCL4, IL-5, IL- 6, IL-21 and IL-22 were involved in the pathway of Cytokine-cytokine receptor interaction (Supplementary file: Table S4).. - The DNA methylation mainly occurred in CG context but rarely in non-CG (CHG and CHH) context on all chromosomes or genome functional regions of chicken, which was consistent with the DNA methylation profile in mammals [41]. - The methyla- tion in the promoter generally induces transcription re- pression [42]. - In the current study, DNA methylation level in the gene body was higher than that in the gene initiation and gene termination regions, which was con- sistent with the previous results [43, 44]. - The collective results suggest the methylation in the gene body regions may play an important role in regulating gene expression.. - 2 DNA methylation levels in functional regions of the genome. - The closer the site in the first circle are to the center, the greater the number of DMC. - The number of hyper-methylated genes in the inocu- lated group was higher than that of hypo-methylated genes across all chromosomes rather than Chr16 and W.. - In the current study, DMGs were mainly involved in metabolism process and immune system process, which was consistent with those previous results. - Variation in the methylation state of inflammatory bowel disease (IBD)-associated genes alters gene expression, contributing to disease onset and progression [53]. - The results collectively suggested that DNA methylation could regulate host immune response via regulating. - It has been revealed that circadian rhythm related genes play critical roles in the host response to C. - The methylation variation of rhythmic process- related genes was triggered in chicken following SE inoculation in the current study. - Interestingly, the differentially methylated genes were correlated with immune process, metabolic process and rhythmic process in the current study. - There may exist an interaction among the three processes in the chicken inoculated with SE. - Wnt signaling pathway is involved in the development, cell differentiation and disease pathophysiology [58], and was significantly altered in chicken cecum at the day 4 after Salmonella infection [59]. - TGF-β plays a role in the regulation of inflammation with T cells being a key target [61]. - TGF-β signaling pathway is significantly changed in the chicken cecum at day 4 post S. - mTOR is a sensor and regulator of immunometabolic changes during Salmonella infection in the chicken [59]. - The enriched Wnt signaling path- way, TGF-β signaling pathway and mTOR signaling pathway may indicate that SE inoculation would affect the chicken immune and metabolism through altering gene DNA methylation in related signaling pathways.. - HOX genes, a conserved gene family, play crucial roles in embryonic development and is involved in the reproduction and development of cells [64]. - In the current study, the DMC was detected in 37 genes in HOX gene family, 8 of those genes had higher density than 0.005 and distributed on both Chr2 and Chr7. - Both miRNA and DNA methylation are important fac- tors to regulate gene expression. - DNA methylation can regulate miRNA expression during tumorigenesis [73]. - Methylation-sensitive mir-345 plays a role of antineo- plastic as a growth inhibitor in the development of colo- rectal cancer [78]. - regions of miRNAs in the chicken were highly methyl- ated [25], which was consistent with the current results.. - In the current study, miRNA has the most density DMCs among all genes. - The DMC of 6 tRNAs was higher than 0.10 in the current study. - Methylation of miRNA and HOX gene family may play roles in the epigenetic regulation responding to SE inoculation in chicken. - Re- sults herein would pave the foundation for understand- ing the methylation regulation mechanism of chicken in the response of SE inoculation.. - Jining Bairi chicken, a China local chicken breed with ability of disease and stress resistance, was used in the current study and provided by Shandong Bairi Chicken Breeding Co., Ltd. - Each chicken in the inoculated group was orally inoculated with 0.3 ml 10 9 colony-forming units (cfu)/ml SE inoculant, and each chicken in the control group in- oculated with the same amount of sterile phosphate buf- fer saline (PBS). - Bisulfite conversion was conducted using the EZ DNA Methylation-Gold Kit (Zymo Research, Irvine, CA, USA). - Additional file 4: Supplementary Table S4.The differentially methylated genes in two pathways.. - We thank Hao Zhang for providing the Jining Bairi chicken used in the current study.. - The datasets generated and/or analyzed during the current study are available in the Sequence Read Archive repository with accession number of PRJNA668639. - Prevalence and characterization of salmonellae in commercial ground beef in the United States. - Foodborne illness acquired in the United States--major pathogens. - Dynamic DNA methylation orchestrates cardiomyocyte development, maturation and disease. - Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. - Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. - Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an. - DNA methylation of the first exon is tightly linked to transcriptional silencing.. - How does DNA methylation repress transcription? Trends Genet. - Genome-wide analysis of DNA methylation in bovine placentas. - Genome-wide comparative analysis of DNA methylation between soybean cytoplasmic male-sterile line NJCMS5A and its maintainer NJCMS5B. - High resolution methylome map of rat indicates role of intragenic DNA methylation in identification of coding region. - Genome- wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. - Genome-wide mapping of DNA methylation in chicken. - DNA methylation: a promising landscape for immune system-related diseases.. - Changes of host DNA methylation in domestic chickens infected with Salmonella enterica. - Differences in expression of genes in the MyD88 and TRIF signalling pathways and methylation of TLR4 and TRIF in Tibetan chickens and DaHeng S03 chickens infected with Salmonella enterica serovar enteritidis. - The effect of Salmonella enteritis infection on chicken cecal genomic DNA methylation. - Detection of DNA methylation by whole- genome bisulfite sequencing. - DNA methylation: roles in mammalian development.. - DNA methylation patterns in the hypothalamus of female pubertal goats.. - Aberrant DNA Methylation Is Associated with Disease Progression, Resistance to Imatinib and Shortened Survival in Chronic Myelogenous Leukemia. - The correlated expression of immune and energy metabolism related genes in the response to Salmonella enterica serovar Enteritidis inoculation in chicken. - Identification of disease-associated DNA methylation in intestinal tissues from patients with inflammatory bowel disease. - Cecal CircRNAs are associated with the response to Salmonella Enterica Serovar Enteritidis inoculation in the chicken. - Messenger RNA expression of chicken CLOCK gene in the response to campylobacter jejuni inoculation. - A role for the non-canonical Wnt- β -catenin and TGF- β signaling pathways in the induction of tolerance during the establishment of a Salmonella enterica Serovar Enteritidis persistent Cecal infection in chickens. - Genome-wide DNA methylation profiling of chronic lymphocytic leukemia allows identification of epigenetically repressed molecular pathways with clinical impact. - miRNA Gene Promoters Are Frequent Targets of Aberrant DNA Methylation in Human Breast Cancer.. - The landscape of DNA methylation associated with the transcriptomic network in layers and broilers generates insight into embryonic muscle development in chicken. - visualization and quality control for DNA methylation data from bisulfite sequencing
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