Systematic identification of circular RNAs and corresponding regulatory networks unveil their potential roles in the midguts of eastern honeybee workers

Chen, Dafu; Chen, Huazhi; Du, Yuguang; Zhu, Zhiwei; Wang, Jie; Geng, Suxia; Zheng, Yusheng; Hou, Chunsheng; Diao, Qingyun; Guo, Rui

doi:10.1007/s00253-019-10159-9

Cited by 20 publications

(44 citation statements)

References 82 publications

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“…CircRNAs in AcCK1 and AcCK2 groups had been identified in previous study (Chen et al, 2020a). In this work, circRNAs in AcT1 and AcT2 groups were identified following our previously described method (Chen et al, 2020a). Shortly, clean reads were mapped to the A. cerana reference genome (assembly ACSNU-2.0) using TopHat software (Kim et al, 2013), and 20 nt at both ends of unmapped reads were then extracted and independently mapped to the reference genome; the mapped anchor reads were submitted to find_circ software (Memczak et al, 2013) to perform circRNA identification following criteria: circRNA length < 100 kb, best qual A > 35 or best qual B > 35, anchor overlap ≤ 2, n uniq > 2, edit ≤ 2, n uniq > int (samples/2), and breakpoints = 1.…”

Section: Bioinformatic Prediction Of Circrnasmentioning

confidence: 68%

“…Raw data are available in NCBI Short Read Archive database (http://www.ncbi.nlm.nih.gov/sra/) under BioProject number: PRJNA406998. In total, 1 809 736 786 raw reads were produced from RNA-seq, and 1 562 162 742 clean reads were gained after quality control; the mean Q20 of clean reads from control groups and treatment groups were 94.76% and 94.77%, respectively; the mapping ratio of clean reads to the reference genome of A. cerana were 75.78%(AcCK1), 55.01%(AcCK2), 78.13%(AcT1) and 44.19%(AcT2), respectively (Chen et al, 2020a; Fu et al, 2020).…”

Section: Methodsmentioning

confidence: 99%

“…In combination with previously identified miRNAs based on sRNA-seq data (Chen et al, 2019a), target miRNAs of DEcircRNAs were predicted on basis of the previously described protocol by Chen et al (2020a). Briefly, according to the criteria of P ≤ 0.05 and free energy ≤ -35 kcal/mol, potential target miRNAs of DEcircRNAs were predicted using three software including mireap, miranda (v3.3a) and targetscan (version: 7.0), followed by construction of DEcircRNA-miRNA regulatory network; further, target mRNAs of DEcircRNAs-targeted miRNAs were predicted and then DEcircRNA-miRNA-mRNA regulatory network was constructed; the regulatory networks were visualized by Cytoscape software (Smoot et al, 2011) with the default parameter.…”

Section: Methodsmentioning

confidence: 99%

Section: Bioinformatic Prediction Of Circrnasmentioning

confidence: 98%

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CircRNA-regulated immune response of Asian honey bee workers to microsporidian infection

Zhu

Wang

Fan

et al. 2022

Preprint

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Nosema ceranae is a widespread fungal parasite for honey bees, causing bee nosemosis. Based on deep sequencing and bioinformatics, identification of circular RNAs (circRNAs) in Apis cerana cerana workers midguts and circRNA-regulated immune response of host to N. ceranae invasion were conducted in this current work, followed by molecular verification of back-splicing sites and expression trends of circRNAs. Here, 10185 and 7405 circRNAs were identified in the midguts of workers at 7 d (AcT1) and 10 d (AcT2) post inoculation (dpi) with N. ceranae. PCR amplification result verified the back-splicing sites in three specific circRNAs (novel_circ_005123, novel_circ_007177, and novel_circ_015140) expressed in N. ceranae-inoculated midgut. In combination with transcriptome data from corresponding un-inoculated midguts (AcCK1 and AcCK2), 2266 circRNAs were found to be shared by the aforementioned four groups, whereas the numbers of specific ones were 2618, 1917, 5691 and 3723 respectively. Further, 83 (52) differentially expressed circRNAs (DEcircRNAs) were identified in AcCK1 vs AcT1 (AcCK2 vs AcT2) comparison group. Source genes of DEcircRNAs in workers midgut at 7 dpi were involved in two cellular immune-related pathways such as endocytosis and ubiquitin mediated proteolysis. Additionally, competing endogenous RNA network analysis showed that 23 (13) DEcircRNAs in AcCK1 vs AcT1 (AcCK2 vs AcT2) can target 18 (14) miRNAs and further link to 1111 (1093) mRNAs. These target mRNAs were annotated to six cellular immunity pathways including endocytosis, lysosome, phagosome, ubiquitin mediated proteolysis, metabolism of xenobiotics by cytochrome P450, and insect hormone biosynthesis. Moreover, 284 (164) IRES and 54 (26) ORF were identified from DEcircRNAs in AcCK1 vs AcT1 (AcCK2 vs AcT2) comparison group; additionally, ORFs in DEcircRNAs in midgut at 7 dpi with N. ceranae were associated with several crucial pathways including endocytosis and ubiquitin-mediated proteolysis. Finally, RT-qPCR results showed that the expression trends of six DEcircRNAs were consistent with those in transcriptome data. These results demonstrated that N. ceranae altered the expression pattern of circRNAs in A. c. cerana workers midguts, and DEcircRNAs were likely to regulate host cellular and humoral immune response to microsporidian infection. Our findings lay a foundation for clarifying the mechanism underlying host immune response to N. ceranae infection and provide a new insight into interaction between Asian honey bee and microsporidian.

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Section: Bioinformatic Prediction Of Circrnasmentioning

confidence: 68%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Bioinformatic Prediction Of Circrnasmentioning

confidence: 98%

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CircRNA-regulated immune response of Asian honey bee workers to microsporidian infection

Zhu

Wang

Fan

et al. 2022

Preprint

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“…MicroRNA (miRNA) is a class of small (18–24 nt), single-strand, and endogenous ncRNA that plays important roles in the post-transcriptional regulation of target gene expression [ 16 , 17 ] related to various biological processes, such as tissue development [ 18 ]. Previous studies on honeybee miRNAs revealed their key roles in mediating diverse physiological processes, such as caste differentiation [ 19 , 20 ], division of labor [ 21 , 22 ], memory formation [ 23 , 24 ], queen reproductive performance [ 25 , 26 ], immune defense [ 27 , 28 ], and embryonic and midgut development [ 29 , 30 ]. However, little is known about whether/how miRNAs regulate the HPGs development in worker bees.…”

Section: Introductionmentioning

confidence: 99%

Age and Behavior-Dependent Differential miRNAs Expression in the Hypopharyngeal Glands of Honeybees (Apis mellifera L.)

Shi

Zhu

Liu

et al. 2021

Insects

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This study aims to investigate the expression differences of miRNAs in the hypopharyngeal glands (HPGs) of honeybees at three developmental stages and to explore their regulation functions in the HPGs development. Small RNA sequencing was employed to analyze the miRNA profiles of HPGs in newly-emerged bees (NEB), nurse bees (NB), and forager bees (FB). Results showed that a total of 153 known miRNAs were found in the three stages, and ame-miR-276-3p, ame-miR-375-3p, ame-miR-14-3p, ame-miR-275-3p, and ame-miR-3477-5p were the top five most abundant ones. Furthermore, the expression of 11 miRNAs, 17 miRNAs, and 18 miRNAs were significantly different in NB vs. FB comparison, NB vs. NEB comparison, and in FB vs. NEB comparison, respectively, of which ame-miR-184-3p and ame-miR-252a-5p were downregulated in NB compared with that in both the FB and NEB, while ame-miR-11-3p, ame-miR-281-3p, and ame-miR-31a-5p had lower expression levels in FB compared with that in both the NB and NEB. Bioinformatic analysis showed that the potential target genes of the differentially expressed miRNAs (DEMs) were mainly enriched in several key signaling pathways, including mTOR signaling pathway, MAPK signaling pathway-fly, FoxO signaling pathway, Hippo signaling pathway-fly. Overall, our study characterized the miRNA profiles in the HPGs of honeybees at three different developmental stages and provided a basis for further study of the roles of miRNAs in HPGs development.

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Dynamics and regulatory role of circRNAs in Asian honey bee larvae following fungal infection

Guo,

Zhang,

Zang

et al. 2024

Appl Microbiol Biotechnol

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Non-coding RNA (ncRNA) plays a vital part in the regulation of immune responses, growth, and development in plants and animals. Here, the identification, characteristic analysis, and molecular verification of circRNAs in Apis cerana cerana worker larval guts were conducted, followed by in-depth investigation of the expression pattern of larval circRNAs during Ascosphaera apis infection and exploration of the potential regulatory part of differentially expressed circRNAs (DEcircRNAs) in host immune responses. A total of 3178 circRNAs in the larval guts of A. c. cerana were identified, with a length distribution ranging from 15 to 96,007 nt. Additionally, 155, 95, and 86 DEcircRNAs were identified in the in the 4-, 5-, and 6-day-old larval guts following A. apis infection. These DEcircRNAs were predicted to target 29, 25, and 18 parental genes relevant to 12, 20, and 17 GO terms as well as 144, 114, and 61 KEGG pathways, including 5 cellular and 4 humoral immune pathways. Complex competing endogenous RNA (ceRNA) regulatory networks were detected as being formed among DEcircRNAs, DEmiRNAs, and DEmRNAs. The target DEmRNAs were engaged in 36, 47, and 47 GO terms as well as 331, 332, and 331 pathways, including 6 cellular and 6 humoral immune pathways. Further, 19 DEcircRNAs, 5 DEmiRNAs, and 3 mRNAs were included in the sub-networks relative to 3 antioxidant enzymes. Finally, back-splicing sites within 15 circRNAs and the difference in the 15 DEcircRNAs’ expression between uninoculated and A. apis–inoculated larval guts were confirmed based on molecular methods. These findings not only enrich our understanding of bee host–fungal pathogen interactions but also lay a foundation for illuminating the mechanism underlying the DEcircRNA-mediated immune defense of A. c. cerana larvae against A. apis invasion. Key points • The expression pattern of circRNAs was altered in the A. cerana worker larval guts following A. apis infection. • Back-splicing sites within 15 A. cerana circRNAs were verified using molecular approaches. DEcircRNAs potentially modulated immune responses and antioxidant enzymes in A. apis–challenged host guts.

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Systematic identification of circular RNAs and corresponding regulatory networks unveil their potential roles in the midguts of eastern honeybee workers

Cited by 20 publications

References 82 publications

CircRNA-regulated immune response of Asian honey bee workers to microsporidian infection

CircRNA-regulated immune response of Asian honey bee workers to microsporidian infection

Age and Behavior-Dependent Differential miRNAs Expression in the Hypopharyngeal Glands of Honeybees (Apis mellifera L.)

Dynamics and regulatory role of circRNAs in Asian honey bee larvae following fungal infection

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