Stage-specific RNA regulomes of Trichophyton mentagrophytes: mRNA-lncRNA-miRNA interplay in spore-hypha transition
Authors/Creators
- 1. Southwest Medical University, Luzhou, China
- 2. Sichuan University, Chengdu, China
- 3. Changchun Sci-Tech University, Changchun, China
- 4. Luzhou People's Hospital, Luzhou, China
Description
Background: As a globally distributed dermatophyte, Trichophyton mentagrophytes (T. mentagrophytes) causes diverse dermatophytoses in humans and animals. Long non-coding RNAs (lncRNAs) and microRNAs (miRNAs), which serve as critical regulators of diverse biological processes, have been extensively characterized in numerous fungal species. However, the role of mRNAs, lncRNAs, and miRNAs during T. mentagrophytes germination remains unexplored.
Objectives: In this study, the molecular mechanisms involved in the germination of T. mentagrophytes were systematically investigated.
Methods: RNA-sequencing technology, small RNA-sequencing technology, related bioinformatics methods, and qRT-PCR were used to systematically characterize the expression profiles of mRNAs, miRNAs, and lncRNAs in T. mentagrophytes spores and hyphae, and analyze the regulatory mechanisms of mRNAs, miRNAs, and lncRNAs during T. mentagrophytes germination.
Results: In our study, RNA-sequencing was performed to identify mRNAs, lncRNAs, and miRNAs in spores and hyphae of T. mentagrophytes. A total of 3,193 differentially expressed mRNAs, 409 differentially expressed lncRNAs, and 119 differentially expressed miRNAs were identified, with qRT-PCR subsequently used to verify the dependability of the sequencing data. In addition, an mRNA-lncRNA-miRNA regulatory network containing 2,672 mRNAs, 107 miRNAs, and 329 lncRNAs was constructed. Gene Ontology, Kyoto Encyclopedia of Genes and Genomes, and Gene Set Enrichment Analysis suggested that mRNAs, lncRNAs, and miRNAs may play important roles during spore germination, potentially participating in fundamental biosynthetic, cell wall remodelling, cell cycle regulation, cytoskeletal reorganization, epigenetic regulation, and metabolic processes.
Conclusion: Our study revealed the characteristics of mRNAs, lncRNAs, and miRNAs in T. mentagrophytes using transcriptomic methods, and set the stage for future pathogenicity studies and antifungal drug development for T. mentagrophytes.
Files
imafungus_article_166433.pdf
Files
(8.9 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:d26f11240eb20548df2c06b1bbf9dc84
|
8.9 MB | Preview Download |
System files
(237.4 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:94a75df9831ce268ad95690b189319d6
|
237.4 kB | Download |
Linked records
Additional details
References
- Bitencourt TA, Neves-da-Rocha J, Martins MP et al. (2021) StuA-Regulated Processes in the Dermatophyte Trichophyton rubrum: Transcription Profile, Cell-Cell Adhesion, and Immunomodulation. Frontiers in Cellular and Infection Microbiology 11: 643659. https://doi.org/10.3389/fcimb.2021.643659
- Bleichrodt RJ, Foster P, Howell G et al. (2020) Cell wall composition heterogeneity between single cells in Aspergillus fumigatus leads to heterogeneous behavior during antifungal treatment and phagocytosis. mBio 11(3): e03015-19. https://doi.org/10.1128/mBio.03015-19
- Bowman SM, Piwowar A, Al Dabbous M et al. (2006) Mutational analysis of the glycosylphosphatidylinositol (GPI) anchor pathway demonstrates that GPI-anchored proteins are required for cell wall biogenesis and normal hyphal growth in Neurospora crassa. Eukaryotic Cell 5(3): 587–600. https://doi.org/10.1128/EC.5.3.587-600.2006
- Browning H, Hackney DD (2005) The EB1 homolog Mal3 stimulates the ATPase of the kinesin Tea2 by recruiting it to the microtubule. The Journal of Biological Chemistry 280(13): 12299–12304. https://doi.org/10.1074/jbc.M413620200
- Cesana M, Cacchiarelli D, Legnini I et al. (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147(2): 358–369. https://doi.org/10.1016/j.cell.2011.09.028
- Chardwiriyapreecha S, Shimazu M, Morita T et al. (2008) Identification of the fnx1+ and fnx2+ genes for vacuolar amino acid transporters in Schizosaccharomyces pombe. FEBS Letters 582(15): 2225–2230. https://doi.org/10.1016/j.febslet.2008.05.017
- Chen LL, Kim VN (2024) Small and long non-coding RNAs: Past, present, and future. Cell 187(23): 6451–6485. https://doi.org/10.1016/j.cell.2024.10.024
- Chen H, Wang Z, Wang Z et al. (2016) Improving methionine and ATP availability by MET6 and SAM2 co-expression combined with sodium citrate feeding enhanced SAM accumulation in Saccharomyces cerevisiae. World Journal of Microbiology & Biotechnology 32(4): 56. https://doi.org/10.1007/s11274-016-2010-y
- Chen S, Zhou Y, Chen Y et al. (2018) fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England) 34(17): i884–i890. https://doi.org/10.1093/bioinformatics/bty560
- Chermette R, Ferreiro L, Guillot J (2008) Dermatophytoses in animals. Mycopathologia 166(5–6): 385–405. https://doi.org/10.1007/s11046-008-9102-7
- Cieśla M, Mierzejewska J, Adamczyk M et al. (2014) Fructose bisphosphate aldolase is involved in the control of RNA polymerase III-directed transcription. Biochimica et Biophysica Acta. Molecular Cell Research 1843(6): 1103–1110. https://doi.org/10.1016/j.bbamcr.2014.02.007
- Cloutier SC, Wang S, Ma WK et al. (2016) Regulated formation of lncRNA-DNA hybrids enables faster transcriptional induction and environmental adaptation. Molecular Cell 61(3): 393–404. https://doi.org/10.1016/j.molcel.2015.12.024
- Cumsky MG, McEwen JE, Ko C et al. (1983) Nuclear genes for mitochondrial proteins. Identification and isolation of a structural gene for subunit V of yeast cytochrome c oxidase. The Journal of Biological Chemistry 258(22): 13418–13421. https://doi.org/10.1016/S0021-9258(17)43929-9
- de Curcio JS, Oliveira LN, Batista MP et al. (2021) MiRNAs regulate iron homeostasis in Paracoccidioides brasiliensis. Microbes and Infection 23(2–3): 104772. https://doi.org/10.1016/j.micinf.2020.10.008
- Duek L, Kaufman G, Ulman Y et al. (2004) The pathogenesis of dermatophyte infections in human skin sections. The Journal of Infection 48(2): 175–180. https://doi.org/10.1016/j.jinf.2003.09.008
- Ebert A, Monod M, Salamin K et al. (2020) Alarming India-wide phenomenon of antifungal resistance in dermatophytes: A multicentre study. Mycoses 63(7): 717–728. https://doi.org/10.1111/myc.13091
- Elavarashi E, Kindo AJ, Rangarajan S (2017) Enzymatic and non-enzymatic virulence activities of dermatophytes on solid media. Journal of Clinical and Diagnostic Research 11: Dc23–Dc25. https://doi.org/10.7860/JCDR/2017/23147.9410
- Elowe S (2011) Bub1 and BubR1: At the interface between chromosome attachment and the spindle checkpoint. Molecular and Cellular Biology 31(15): 3085–3093. https://doi.org/10.1128/MCB.05326-11
- Fang J, Hogan GJ, Liang G et al. (2007) The Saccharomyces cerevisiae histone demethylase Jhd1 fine-tunes the distribution of H3K36me2. Molecular and Cellular Biology 27(13): 5055–5065. https://doi.org/10.1128/MCB.00127-07
- Fernandez J, Wilson RA (2014) Cells in cells: Morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. Protoplasma 251(1): 37–47. https://doi.org/10.1007/s00709-013-0541-8
- Fernandez J, Marroquin-Guzman M, Wilson RA (2014) Evidence for a transketolase-mediated metabolic checkpoint governing biotrophic growth in rice cells by the blast fungus Magnaporthe oryzae. PLOS Pathogens 10(9): e1004354. https://doi.org/10.1371/journal.ppat.1004354
- Friend JE, Sayyad WA, Arasada R et al. (2018) Fission yeast Myo2: Molecular organization and diffusion in the cytoplasm. Cytoskeleton 75(4): 164–173. https://doi.org/10.1002/cm.21425
- Galvão-Rocha FM, Rocha CHL, Martins MP et al. (2023) The antidepressant sertraline affects cell signaling and metabolism in Trichophyton rubrum. Journal of Fungi (Basel, Switzerland) 9(2): 275. https://doi.org/10.3390/jof9020275
- Govindan B, Bowser R, Novick P (1995) The role of Myo2, a yeast class V myosin, in vesicular transport. The Journal of Cell Biology 128(6): 1055–1068. https://doi.org/10.1083/jcb.128.6.1055
- Harris SD (2005) Morphogenesis in germinating Fusarium graminearum macroconidia. Mycologia 97(4): 880–887. https://doi.org/10.1080/15572536.2006.11832779
- Hashida-Okado T, Ogawa A, Endo M et al. (1996) AUR1, a novel gene conferring aureobasidin resistance on Saccharomyces cerevisiae: A study of defective morphologies in Aur1p-depleted cells. Molecular & General Genetics 251(2): 236–244. https://doi.org/10.1007/BF02172923
- Hiraishi H, Miyake T, Ono B (2008) Transcriptional regulation of Saccharomyces cerevisiae CYS3 encoding cystathionine gamma-lyase. Current Genetics 53(4): 225–234. https://doi.org/10.1007/s00294-008-0181-2
- Hirozumi K, Nakajima H, Machida M et al. (1999) Cloning and characterization of a gene (arpA) from Aspergillus oryzae encoding an actin-related protein required for normal nuclear distribution and morphology of conidiophores. Molecular & General Genetics 262(4–5): 758–767. https://doi.org/10.1007/s004380051138
- Hombach S, Kretz M (2016) Non-coding RNAs: Classification, biology and functioning. Advances in Experimental Medicine and Biology 937: 3–17. https://doi.org/10.1007/978-3-319-42059-2_1
- Horng JS, Linz JE, Pestka JJ (1989) Cloning and characterization of the trpC gene from an aflatoxigenic strain of Aspergillus parasiticus. Applied and Environmental Microbiology 55(10): 2561–2568. https://doi.org/10.1128/aem.55.10.2561-2568.1989
- Hrdlickova R, Toloue M, Tian B (2017) RNA-Seq methods for transcriptome analysis. Wiley Interdisciplinary Reviews. RNA 8(1): e1364. https://doi.org/10.1002/wrna.1364
- Huang P, Yu X, Liu H et al. (2024) Regulation of TRI5 expression and deoxynivalenol biosynthesis by a long non-coding RNA in Fusarium graminearum. Nature Communications 15(1): 1216. https://doi.org/10.1038/s41467-024-45502-w
- Iwakawa HO, Tomari Y (2022) Life of RISC: Formation, action, and degradation of RNA-induced silencing complex. Molecular Cell 82(1): 30–43. https://doi.org/10.1016/j.molcel.2021.11.026
- Karnik R, Zhang B, Waghmare S et al. (2015) Binding of SEC11 indicates its role in SNARE recycling after vesicle fusion and identifies two pathways for vesicular traffic to the plasma membrane. The Plant Cell 27(3): 675–694. https://doi.org/10.1105/tpc.114.134429
- Karuppiah V, Zhang C, Liu T et al. (2023) Transcriptome analysis of T. asperellum GDFS 1009 revealed the role of MUP1 gene on the methionine-based induction of morphogenesis and biological control activity. Journal of Fungi (Basel, Switzerland) 9(2): 215. https://doi.org/10.3390/jof9020215
- Kim D, Langmead B, Salzberg SL (2015) HISAT: A fast spliced aligner with low memory requirements. Nature Methods 12(4): 357–360. https://doi.org/10.1038/nmeth.3317
- Kim GL, Lee S, Luong TT et al. (2017) Effect of decreased BCAA synthesis through disruption of ilvC gene on the virulence of Streptococcus pneumoniae. Archives of Pharmacal Research 40(8): 921–932. https://doi.org/10.1007/s12272-017-0931-0
- Kong L, Zhang Y, Ye ZQ et al. (2007) CPC: Assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Research 35(suppl_2): W345–W349. https://doi.org/10.1093/nar/gkm391
- Lai T, Yu Q, Pan J et al. (2023) The identification and comparative analysis of non-coding RNAs in spores and mycelia of Penicillium expansum. Journal of Fungi (Basel, Switzerland) 9(10): 999. https://doi.org/10.3390/jof9100999
- Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nature Methods 9(4): 357–359. https://doi.org/10.1038/nmeth.1923
- Lau AYT, Xie Y, Cheung MK et al. (2020) Genome-wide mRNA and miRNA analysis in the early stages of germ tube outgrowth in Coprinopsis cinerea. Fungal Genetics and Biology 142: 103416. https://doi.org/10.1016/j.fgb.2020.103416
- Li B, Dewey CN (2011) RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12(1): 323. https://doi.org/10.1186/1471-2105-12-323
- Li P, Ruan X, Yang L et al. (2015) A liver-enriched long non-coding RNA, lncLSTR, regulates systemic lipid metabolism in mice. Cell Metabolism 21(3): 455–467. https://doi.org/10.1016/j.cmet.2015.02.004
- Li Y, Syed J, Sugiyama H (2016) RNA-DNA triplex formation by long noncoding RNAs. Cell Chemical Biology 23(11): 1325–1333. https://doi.org/10.1016/j.chembiol.2016.09.011
- Li Y, Xian H, Xu Y et al. (2021) Fine tuning the glycolytic flux ratio of EP-bifido pathway for mevalonate production by enhancing glucose-6-phosphate dehydrogenase (Zwf) and CRISPRi suppressing 6-phosphofructose kinase (PfkA) in Escherichia coli. Microbial Cell Factories 20(1): 32. https://doi.org/10.1186/s12934-021-01526-1
- Liu T, Zhang Q, Wang L et al. (2007) The use of global transcriptional analysis to reveal the biological and cellular events involved in distinct development phases of Trichophyton rubrum conidial germination. BMC Genomics 8(1): 100. https://doi.org/10.1186/1471-2164-8-100
- Liu H, Zhang S, Ma J et al. (2015) Two Cdc2 kinase genes with distinct functions in vegetative and infectious hyphae in Fusarium graminearum. PLOS Pathogens 11(6): e1004913. https://doi.org/10.1371/journal.ppat.1004913
- Liu B, Xiang W, Liu J et al. (2021) The regulatory role of antisense lncRNAs in cancer. Cancer Cell International 21(1): 459. https://doi.org/10.1186/s12935-021-02168-4
- Liu H, Li D, Sun L et al. (2022a) Interaction of lncRNA MIR100HG with hnRNPA2B1 facilitates m(6)A-dependent stabilization of TCF7L2 mRNA and colorectal cancer progression. Molecular Cancer 21(1): 74. https://doi.org/10.1186/s12943-022-01555-3
- Liu N, Xu Y, Li Q et al. (2022b) A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth. Cell Host & Microbe 30(8): 1124–1138. https://doi.org/10.1016/j.chom.2022.07.001
- Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods: A Companion to Methods in Enzymology 25(4): 402–408. https://doi.org/10.1006/meth.2001.1262
- Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15(12): 550. https://doi.org/10.1186/s13059-014-0550-8
- Lu X, Xu Q, Tong Y et al. (2022) Long non-coding RNA EVADR induced by Fusobacterium nucleatum infection promotes colorectal cancer metastasis. Cell Reports 40(3): 111127. https://doi.org/10.1016/j.celrep.2022.111127
- Luzzani C, Cardillo SB, Bermúdez Moretti M et al. (2007) New insights into the regulation of the Saccharomyces cerevisiae UGA4 gene: Two parallel pathways participate in carbon-regulated transcription. Microbiology (Reading, England) 153(11): 3677–3684. https://doi.org/10.1099/mic.0.2007/010231-0
- Mackowiak SD (2011) Identification of novel and known miRNAs in deep-sequencing data with miRDeep2. Curr Protoc Bioinformatics Chapter 12: 12.10.11–12.10.15. https://doi.org/10.1002/0471250953.bi1210s36
- Maddi A, Bowman SM, Free SJ (2009) Trifluoromethanesulfonic acid-based proteomic analysis of cell wall and secreted proteins of the ascomycetous fungi Neurospora crassa and Candida albicans. Fungal Genetics and Biology 46(10): 768–781. https://doi.org/10.1016/j.fgb.2009.06.005
- Masuda H, Toda T, Miyamoto R et al. (2006) Modulation of Alp4 function in Schizosaccharomyces pombe induces novel phenotypes that imply distinct functions for nuclear and cytoplasmic gamma-tubulin complexes. Genes to Cells 11(4): 319–336. https://doi.org/10.1111/j.1365-2443.2006.00946.x
- Masuda H, Fong CS, Ohtsuki C et al. (2011) Spatiotemporal regulations of Wee1 at the G2/M transition. Molecular Biology of the Cell 22(5): 555–569. https://doi.org/10.1091/mbc.e10-07-0644
- Mellado E, Dubreucq G, Mol P et al. (2003) Cell wall biogenesis in a double chitin synthase mutant (chsG-/chsE-) of Aspergillus fumigatus. Fungal Genetics and Biology 38(1): 98–109. https://doi.org/10.1016/S1087-1845(02)00516-9
- Nahkuri S, Paro R (2012) The role of noncoding RNAs in chromatin regulation during differentiation. Wiley Interdisciplinary Reviews. Developmental Biology 1(5): 743–752. https://doi.org/10.1002/wdev.41
- Novačić A, Vučenović I, Primig M et al. (2020) Non-coding RNAs as cell wall regulators in Saccharomyces cerevisiae. Critical Reviews in Microbiology 46(1): 15–25. https://doi.org/10.1080/1040841X.2020.1715340
- Oakley BR (2004) Tubulins in Aspergillus nidulans. Fungal Genetics and Biology 41(4): 420–427. https://doi.org/10.1016/j.fgb.2003.11.013
- Orasch T, Dietl AM, Shadkchan Y et al. (2019) The leucine biosynthetic pathway is crucial for adaptation to iron starvation and virulence in Aspergillus fumigatus. Virulence 10(1): 925–934. https://doi.org/10.1080/21505594.2019.1682760
- Osherov N, May G (2000) Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. Genetics 155(2): 647–656. https://doi.org/10.1093/genetics/155.2.647
- Pascon RC, Ganous TM, Kingsbury JM et al. (2004) Cryptococcus neoformans methionine synthase: Expression analysis and requirement for virulence. Microbiology (Reading, England) 150(9): 3013–3023. https://doi.org/10.1099/mic.0.27235-0
- Pertea M, Pertea GM, Antonescu CM et al. (2015) StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology 33(3): 290–295. https://doi.org/10.1038/nbt.3122
- Rampitsch C, Tinker NA, Subramaniam R et al. (2012) Phosphoproteome profile of Fusarium graminearum grown in vitro under nonlimiting conditions. Proteomics 12(7): 1002–1005. https://doi.org/10.1002/pmic.201100065
- Rödel C, Jupitz T, Schmidt H (1997) Complementation of the DNA repair-deficient swi10 mutant of fission yeast by the human ERCC1 gene. Nucleic Acids Research 25(14): 2823–2827. https://doi.org/10.1093/nar/25.14.2823
- Saçar Demirci MD (2020) Computational prediction of microRNAs in Histoplasma capsulatum. Microbial Pathogenesis 148: 104433. https://doi.org/10.1016/j.micpath.2020.104433
- Salmena L, Poliseno L, Tay Y et al. (2011) A ceRNA hypothesis: The Rosetta Stone of a hidden RNA language? Cell 146(3): 353–358. https://doi.org/10.1016/j.cell.2011.07.014
- Shannon P, Markiel A, Ozier O et al. (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research 13(11): 2498–2504. https://doi.org/10.1101/gr.1239303
- Shuman S (2020) Transcriptional interference at tandem lncRNA and protein-coding genes: An emerging theme in regulation of cellular nutrient homeostasis. Nucleic Acids Research 48(15): 8243–8254. https://doi.org/10.1093/nar/gkaa630
- Sousa S, McLaughlin MM, Pereira SA et al. (2002) The ARO4 gene of Candida albicans encodes a tyrosine-sensitive DAHP synthase: Evolution, functional conservation and phenotype of Aro3p-, Aro4p-deficient mutants. Microbiology (Reading, England) 148(5): 1291–1303. https://doi.org/10.1099/00221287-148-5-1291
- Steyer JT, Todd RB (2023) Branched-chain amino acid biosynthesis in fungi. Essays in Biochemistry 67(5): 865–876. https://doi.org/10.1042/EBC20230003
- Steyer JT, Downes DJ, Hunter CC et al. (2021) Duplication and functional divergence of branched-chain amino acid biosynthesis genes in Aspergillus nidulans. mBio 12(3): e0076821. https://doi.org/10.1128/mBio.00768-21
- Subramanian A, Tamayo P, Mootha VK et al. (2005) Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 102(43): 15545–15550. https://doi.org/10.1073/pnas.0506580102
- Sun J, Li H, Sun X et al. (2012) Trisporic acid stimulates gene transcription of terpenoid biosynthesis in Blakeslea trispora. Process Biochemistry (Barking, London, England) 47(12): 1889–1893. https://doi.org/10.1016/j.procbio.2012.06.017
- Sun L, Luo H, Bu D et al. (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Research 41(17): e166. https://doi.org/10.1093/nar/gkt646
- Szklarczyk D, Franceschini A, Wyder S et al. (2015) STRING v10: Protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Research 43(D1): D447–D452. https://doi.org/10.1093/nar/gku1003
- Tafer H, Hofacker IL (2008) RNAplex: A fast tool for RNA-RNA interaction search. Bioinformatics (Oxford, England) 24(22): 2657–2663. https://doi.org/10.1093/bioinformatics/btn193
- Trapnell C, Williams BA, Pertea G et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28(5): 511–515. https://doi.org/10.1038/nbt.1621
- Wang L, Xu X, Yang J et al. (2018) Integrated microRNA and mRNA analysis in the pathogenic filamentous fungus Trichophyton rubrum. BMC Genomics 19(1): 933. https://doi.org/10.1186/s12864-018-5316-3
- Wang Z, Yu Z, He L et al. (2022) Comprehensive analysis of long non-coding RNA expression profiles in Trichophyton mentagrophytes-infected keratinocytes. Microbial Pathogenesis 167: 105565. https://doi.org/10.1016/j.micpath.2022.105565
- Weitzman I, Summerbell RC (1995) The dermatophytes. Clinical Microbiology Reviews 8(2): 240–259. https://doi.org/10.1128/CMR.8.2.240
- Westfall PJ, Momany M (2002) Aspergillus nidulans septin AspB plays pre- and postmitotic roles in septum, branch, and conidiophore development. Molecular Biology of the Cell 13(1): 110–118. https://doi.org/10.1091/mbc.01-06-0312
- Wu H, Cen Y, Lu Y et al. (2024) Role of chitin synthases CHS1 and CHS2 in biosynthesis of the cyst wall of Cryptocaryon irritans. International Journal of Biological Macromolecules 280: 136143. https://doi.org/10.1016/j.ijbiomac.2024.136143
- Wucher V, Legeai F, Hédan B et al. (2017) FEELnc: A tool for long non-coding RNA annotation and its application to the dog transcriptome. Nucleic Acids Research 45: e57. https://doi.org/10.1093/nar/gkw1306
- Yan P, Luo S, Lu JY et al. (2017) Cis- and trans-acting lncRNAs in pluripotency and reprogramming. Current Opinion in Genetics & Development 46: 170–178. https://doi.org/10.1016/j.gde.2017.07.009
- Yoon JH, Abdelmohsen K, Gorospe M (2013) Posttranscriptional gene regulation by long noncoding RNA. Journal of Molecular Biology 425(19): 3723–3730. https://doi.org/10.1016/j.jmb.2012.11.024
- Zang F, Wang Z, Yang Y et al. (2024) Responses of keratinocytes to Trichophyton mentagrophytes infection based on whole transcriptome analysis. Mycoses 67(3): e13713. https://doi.org/10.1111/myc.13713
- Zhang J, Zeng L, Wu Z et al. (2023) Genome-wide identification and functional analysis of circRNAs in Trichophyton mentagrophytes spores and hyphae. Microbial Pathogenesis 176: 106003. https://doi.org/10.1016/j.micpath.2023.106003