Genome-Wide Identification of Circular RNAs in Fungal Parasite Nosema ceranae

Guo, Rui; Chen, Dafu; Chen, Huazhi; Xiong, Chuan; Zheng, Yusheng; Hou, Chunsheng; Du, Yuguang; Geng, Suxia; Wang, Haipeng; Zhou, Dingding; Guo, Yang

doi:10.1007/s00284-018-1576-z

Cited by 23 publications

(21 citation statements)

References 36 publications

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“…However, little is known about the profiling and role of other ncRNAs such as lncRNAs and circular RNAs involved in interactions between honeybee and microspodian. More recently, our group identified lncRNAs and circRNAs in N. ceranae based on bioinformatics and preliminarily verified their expressions using molecular method [33,90]. Here, based on these previous works, we for the first time used rRNA removal and strand-specific RNA sequencing to systematically characterize and identify lncRNAs involved in the responses of A. m. ligustica to N. ceranae infection.…”

Section: Discussionmentioning

confidence: 99%

Genome-Wide Identification of Long Non-Coding RNAs and Their Regulatory Networks Involved in Apis mellifera ligustica Response to Nosema ceranae Infection

Chen

et al. 2019

Insects

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Long non-coding RNAs (lncRNAs) are a diverse class of transcripts that structurally resemble mRNAs but do not encode proteins, and lncRNAs have been proven to play pivotal roles in a wide range of biological processes in animals and plants. However, knowledge of expression patterns and potential roles of honeybee lncRNA response to Nosema ceranae infection is completely unknown. Here, we performed whole transcriptome strand-specific RNA sequencing of normal midguts of Apis mellifera ligustica workers (Am7CK, Am10CK) and N. ceranae-inoculated midguts (Am7T, Am10T), followed by comprehensive analyses using bioinformatic and molecular approaches. A total of 6353 A. m. ligustica lncRNAs were identified, including 4749 conserved lncRNAs and 1604 novel lncRNAs. These lncRNAs had minimal sequence similarities with other known lncRNAs in other species; however, their structural features were similar to counterparts in mammals and plants, including shorter exon and intron length, lower exon number, and lower expression level, compared with protein-coding transcripts. Further, 111 and 146 N. ceranae-responsive lncRNAs were identified from midguts at 7-days post-inoculation (dpi) and 10 dpi compared with control midguts. Twelve differentially expressed lncRNAs (DElncRNAs) were shared by Am7CK vs. Am7T and Am10CK vs. Am10T comparison groups, while the numbers of unique DElncRNAs were 99 and 134, respectively. Functional annotation and pathway analysis showed that the DElncRNAs may regulate the expression of neighboring genes by acting in cis and trans fashion. Moreover, we discovered 27 lncRNAs harboring eight known miRNA precursors and 513 lncRNAs harboring 2257 novel miRNA precursors. Additionally, hundreds of DElncRNAs and their target miRNAs were found to form complex competitive endogenous RNA (ceRNA) networks, suggesting that these DElncRNAs may act as miRNA sponges. Furthermore, DElncRNA-miRNA-mRNA networks were constructed and investigated, the results demonstrated that a portion of the DElncRNAs were likely to participate in regulating the host material and energy metabolism as well as cellular and humoral immune host responses to N. ceranae invasion. Our findings revealed here offer not only a rich genetic resource for further investigation of the functional roles of lncRNAs involved in the A. m. ligustica response to N. ceranae infection, but also a novel insight into understanding the host-pathogen interaction during honeybee microsporidiosis.

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Section: Discussionmentioning

confidence: 99%

Genome-Wide Identification of Long Non-Coding RNAs and Their Regulatory Networks Involved in Apis mellifera ligustica Response to Nosema ceranae Infection

Chen

et al. 2019

Insects

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“…Clean spores of N. ceranae were previously purified using Percoll discontinuous gradient centrifugation protocol and preserved in Honeybee Protection Laboratory [18], College of Animal Sciences (College of Bee Science). A. c. cerana workers were selected from three colonies located in the teaching apiary of the College of Animal Sciences (College of Bee Science) in Fujian Agriculture and Forestry University.…”

Section: Fungal Spore and Honeybeementioning

confidence: 99%

“…Hence, the high-quality RNA-seq data can be used for transcriptomic analyses in the present study. In another work, we conducted deep sequencing of clean spores of N. ceranae (NcCK) using Illumina HiSeq-based RNA-seq [18]. A total of 416, 156, 600 raw reads were produced, and after quality control, 210, 824, 312 clean reads were obtained, with average Q30 of 92.63%, which suggested that the high-quality transcriptome data can be used in this study.…”

Section: Transcriptome Data Sourcementioning

confidence: 99%

“…The copyright holder for this this version posted January 13, 2022. ; https://doi.org/10.1101/2022.01.12.476029 doi: bioRxiv preprint spores [16,17,18]. Recently, we conducted deep sequencing of the midguts of A. c. cerana workers at 7 and 10 days post inoculation (dpi) with N. ceranae spores, and deciphered the host cellular and humoral responses to fungal infection [19]; in addition, we analyzed the expression profile of highly expressed genes (HEGs) and discussed their potential roles in N. ceranae infestation [20].…”

Section: Introductionmentioning

confidence: 99%

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Comparative transcriptome investigation of Nosema ceranae infecting eastern honeybee workers

Chen

Guo

2022

Preprint

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Apis cerana is the original host for Nosema ceranae, a widespread fungal parasite resulting in bee nosemosis, which leads to severe losses for apiculture industry throughout the world. However, knowledge of N. ceranae infecting eastern honeybees is extremely limited. Currently, the mechanism underlying N. ceranae infection is still largely unknown. Based on our previously gained high-quality transcriptome datasets, comparative transcriptomic investigation was conducted in this work, with a focus on virulence factor-associated differentially expressed genes (DEGs). Microscopic observation showed that A. c. cerana workers midguts were effectively infected after inoculation with clean spores of N. ceranae. Totally, 1411, 604, and 38 DEGs were identified from NcCK vs. NcT1, NcCK vs. NcT2 and NcT1 vs. NcT2 comparison groups. Venn analysis showed that ten up-regulated genes and nine down-regulated ones were shared by aforementioned comparison groups. GO category indicated these DEGs were involved in a series of functional terms relevant to biological process, cellular component, and molecular function, such as metabolic process, cell part, and catalytic activity. Additionally, KEGG pathway analysis suggested that the DEGs were engaged in an array of pathways of great importance, such as metabolic pathway, glycolysis, and biosynthesis of secondary metabolites. Further, expression clustering analysis demonstrated that majority of genes encoding virulence factors such as ricin B lectins and polar tube proteins displayed apparent up-regulation, whereas a few virulence factor-associated genes such as hexokinase gene and 6-phosphofructokinase gene presented down-regulation during the fungal infection. Finally, the expression trend of 14 DEGs was confirmed by RT-qPCR, validating the reliability of our transcriptome datasets. These results together demonstrated that an overall alteration of the transcriptome of N. ceranae occurred during the infection of A. c. ceranae workers, and most of virulence factor-related genes were induced to activation to promote the fungal invasion. Our findings not only lay a foundation for clarifying the molecular mechanism underlying N. ceranae infection of eastern honeybee workers, but also shed light on developing novel targets for microsporidiosis control.

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“…The host genes of circRNAs in conidia were involved mainly in the synthesis of storage products for rice infection, while those of circRNAs in mycelia were involved primarily in basic metabolism for the promotion of normal fungal growth [ 28 ]. In addition, Guo et al identified 204 circRNAs in spore samples of the microsporidium species Nosema ceranae , and circRNA-miRNA-mRNA regulatory networks showed that the target genes were engaged in various metabolic pathways, indicating that these circRNAs might play regulatory roles in N. ceranae spores [ 29 ]. However, knowledge about circRNAs in fungi remains from sufficient.…”

Section: Introductionmentioning

confidence: 99%

Genome-wide identification and functional analysis of circRNAs in Trichophyton rubrum conidial and mycelial stages

Cao

Dong

et al. 2022

BMC Genomics

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Background Circular RNAs (circRNAs) are a group of noncoding RNAs that participate in gene expression regulation in various pathways. The essential roles of circRNAs have been revealed in many species. However, knowledge of circRNAs in fungi is still not comprehensive. Results Trichophyton rubrum (T. rubrum) is considered a model organism of human pathogenic filamentous fungi and dermatophytes. In this study, we performed a genome-wide investigation of circRNAs in T. rubrum based on high-throughput sequencing and ultimately identified 4254 circRNAs. Most of these circRNAs were specific to the conidial or mycelial stage, revealing a developmental stage-specific expression pattern. In addition, 940 circRNAs were significantly differentially expressed between the conidial and mycelial stages. PCR experiments conducted on seven randomly selected differentially expressed (DE-) circRNAs confirmed the circularized structures and relative expression levels of these circRNAs. Based on their genome locations, most circRNAs originated from intergenic regions, unlike those in plants and animals. Furthermore, we constructed circRNA-miRNA-mRNA regulatory networks that included 661 DE-circRNAs targeting 140 miRNAs and further regulating 2753 mRNAs. The relative expression levels of two randomly selected circRNA-miRNA-mRNA axes were investigated by qRT-PCR, and the competing endogenous RNA (ceRNA) network theory was validated. Functional enrichment analysis of the target genes suggested that they were significantly involved in posttranscriptional processes and protein synthesis as well as some small-molecule metabolism processes. CircRNAs are relatively more conserved in closely related dermatophytes but rarely conserved in distantly related species. Tru_circ07138_001 is a highly conserved circRNA that was conserved in all ten dermatophytes analyzed in our study and three distantly related species. Its host gene TERG_07138 was also highly conserved in two of these distantly related species Gallus gallus and Caenorhabditis elegans. The specific role of this circRNA deserves further exploration. Conclusions Our study is the first to provide a global profile of circRNAs in T. rubrum as well as dermatophytes. These results could serve as valuable resources for research on circRNA regulatory mechanisms in fungi and reveal new insights for further investigation of the physical characteristics of these significant human fungal pathogens.

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Genome-Wide Identification of Circular RNAs in Fungal Parasite Nosema ceranae

Cited by 23 publications

References 36 publications

Genome-Wide Identification of Long Non-Coding RNAs and Their Regulatory Networks Involved in Apis mellifera ligustica Response to Nosema ceranae Infection

Genome-Wide Identification of Long Non-Coding RNAs and Their Regulatory Networks Involved in Apis mellifera ligustica Response to Nosema ceranae Infection

Comparative transcriptome investigation of Nosema ceranae infecting eastern honeybee workers

Genome-wide identification and functional analysis of circRNAs in Trichophyton rubrum conidial and mycelial stages

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