Identification of Wolbachia-responsive microRNAs in the two-spotted spider mite, Tetranychus urticae

BMC Genomics

Xiao-Yue Hong¹  Kai-Jun Zhang²  Yan-Kai Zhang¹  Xia Rong¹ 

[1] Department of Entomology, College of Plant Protection, Nanjing Agricultural University, Nanjing, Jiangsu, China;Department of Entomology, College of Plant Protection, Southwest University, Chongqing, Chongqing, China

关键词: Gene expression;    miRNAs;    Wolbachia;    Two-spotted spider mite;   

Others  :  1127220
DOI  :  10.1186/1471-2164-15-1122

 received in 2014-08-07, accepted in 2014-12-09,  发布年份 2014

【 摘 要 】

Background

The two-spotted spider mite, Tetranychus urticae, is infected with Wolbachia, which have the ability to manipulate host reproduction and fitness. MicroRNAs (miRNAs) are small non-coding RNAs that are involved in many biological processes such as development, reproduction and host-pathogen interactions. Although miRNA was observed to involve in Wolbachia-host interactions in the other insect systems, its roles have not been fully deciphered in the two-spotted spider mite.

Results

Small RNA libraries of infected and uninfected T. urticae for both sexes (in total four libraries) were constructed. By integrating the mRNA data originated from the same samples, the target genes of the differentially expressed miRNAs were predicted. Then, GO and pathway analyses were performed for the target genes. Comparison of libraries showed that Wolbachia infection significantly regulated 91 miRNAs in females and 20 miRNAs in males, with an overall suppression of miRNAs in Wolbachia-infected libraries. A comparison of the miRNA and mRNA data predicted that the differentially expressed miRNAs negatively regulated 90 mRNAs in females and 9 mRNAs in males. An analysis of target genes showed that Wolbachia-responsive miRNAs regulated genes with function in sphingolipid metabolism, lysosome function, apoptosis and lipid transporting in both sexes, as well as reproduction in females.

Conclusion

Comparisons of the miRNA and mRNA data can help to identify miRNAs and miRNA target genes involving in Wolbachia-host interactions. The molecular targets identified in this study should be useful in further functional studies.

【 授权许可】

   
2014 Rong et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Zug R, Hammerstein P: Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 2012, 7:e38544.
• [2]Ferri E, Bain O, Barbuto M, Martin C, Lo N, Uni S, Landmann F, Baccei SG, Guerrero R, de Souza LS, Bandi C, Wanji S, Diagne M, Casiraghi M: New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PLoS One 2011, 6:e20843.
• [3]Werren JH, Baldo L, Clark ME: Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008, 6:741-751.
• [4]Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA: From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 2007, 5:e114.
• [5]Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T: Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 2010, 107:769-774.
• [6]Li Z, Carlow CK: Characterization of transcription factors that regulate the type IV secretion system and riboflavin biosynthesis in Wolbachia of Brugia malayi. PLoS One 2012, 7:e51597.
• [7]Smibert P, Lai EC: A view from Drosophila: Multiple biological functions for individual microRNAs. Semin Dev Biol 2010, 21:745-753.
• [8]Asgari S: Role of microRNAs in insect host-microorganism interactions. Front Physiol 2011, 2:48.
• [9]Wang XH, Aliyari R, Li WX, Li HW, Kim K, Carthew R, Atkinson P, Ding S-W: RNA interference directs innate immunity against viruses in adult Drosophila. Sci Signal 2006, 312:452.
• [10]Lourenço AP, Guidugli-Lazzarini KR, Freitas FC, Bitondi MM, Simões ZL: Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochem Mol Biol 2013, 43:474-482.
• [11]Bartel DP: MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
• [12]Asgari S: MicroRNA functions in insects. Insect Biochem Mol Biol 2013, 43:388-397.
• [13]Hussaina M, Frentiua FD, Moreiraa LA, O'Neill SL, Asgaria S: Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci U S A 2011, 108:9250-9255.
• [14]Fagegaltier D, Bougé AL, Berry B, Poisot É, Sismeiro O, Coppée JY, Théodore L, Voinnet O, Antoniewski C: The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. Proc Natl Acad Sci U S A 2009, 106:21258-21263.
• [15]Fabian MR, Sonenberg N, Filipowicz W: Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010, 79:351-379.
• [16]Hussain M, O'Neill SL, Asgari S: Wolbachia interferes with the intracellular distribution of Argonaute 1 in the dengue vector Aedes aegypti by manipulating the host microRNAs. RNA Biol 2013, 10:1868-1875.
• [17]Kozomara A, Griffiths-Jones S: miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42:D68-D73.
• [18]Osei-Amo S, Hussain M, O'Neill SL, Asgari S: Wolbachia-induced aae-miR-12 miRNA negatively regulates the expression of MCT1 and MCM6 genes in Wolbachia-infected mosquito cell line. PLoS One 2012, 7:e50049.
• [19]Zhang G, Hussain M, O’Neill SL, Asgari S: Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc Natl Acad Sci U S A 2013, 110:10276-10281.
• [20]Mayoral JG, Etebari K, Hussain M, Khromykh AA, Asgari S: Wolbachia infection modifies the profile, shuttling and structure of microRNAs in a mosquito cell line. PLoS One 2014, 9:e96107.
• [21]Jeppson LR, Keifer HH, Baker EW: Mites Injurious to Economic Plants. Berkeley: University of California Press; 1975.
• [22]Zhao DX, Zhang XF, Chen DS, Zhang YK, Hong XY: Wolbachia-host interactions: host mating patterns affect Wolbachia density dynamics. PLoS One 2013, 8:e66373.
• [23]Ambros V, Bartel B, Bartel DP, Burge CB, Carrington JC, Chen X, Dreyfuss G, Eddy SR, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T: A uniform system for microRNA annotation. RNA 2003, 9:277-279.
• [24]Griffiths-Jones S, Moxon S, Marshall M, Khanna A, Eddy SR, Bateman A: Rfam: annotating non-coding RNAs in complete genomes. Nucleic Acids Res 2005, 33:D121-124.
• [25]Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T: Identification of novel genes coding for small expressed RNAs. Science 2001, 294:853-858.
• [26]Marco A, Hooks K, Griffiths-Jones S: Evolution and function of the extended miR-2 microRNA family. RNA Biol 2012, 9:242-248.
• [27]Leaman D, Chen PY, Fak J, Yalcin A, Pearce M, Unnerstall U, Marks DS, Sander C, Tuschl T, Gaul U: Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 2005, 121:1097-1108.
• [28]Enquist IB, Bianco CL, Ooka A, Nilsson E, Månsson JE, Ehinger M, Richter J, Brady RO, Kirik D, Karlsson S: Murine models of acute neuronopathic Gaucher disease. Proc Natl Acad Sci U S A 2007, 104:17483-17488.
• [29]Jmoudiak M, Futerman AH: Gaucher disease: pathological mechanisms and modern management. Br J Haematol 2005, 129:178-188.
• [30]Bazzocchi C, Comazzi S, Santoni R, Bandi C, Genchi C, Mortarino M: Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol 2007, 29:73-79.
• [31]Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F: Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 2009, 5:e1000630.
• [32]Fast EM, Toomey ME, Panaram K, Desjardins D, Kolaczyk ED, Frydman HM: Wolbachia enhance Drosophila stem cell proliferation and target the germline stem cell niche. Science 2011, 334:990-992.
• [33]Zhukova MV, Kiseleva E: The virulent Wolbachia strain wMelPop increases the frequency of apoptosis in the female germline cells of Drosophila melanogaster. BMC Microbiol 2012, 12 Suppl 1:S15.
• [34]Tram U, Sullivan W: Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 2002, 296:1124-1126.
• [35]Landmann F, Orsi GA, Loppin B, Sullivan W: Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog 2009, 5:e1000343.
• [36]Peterson CL, Laniel MA: Histones and histone modifications. Curr Biol 2004, 14:R546-R551.
• [37]Cao W, Aghajanian HK, Haig-Ladewig LA, Gerton GL: Sorbitol can fuel mouse sperm motility and protein tyrosine phosphorylation via sorbitol dehydrogenase. Biol Reprod 2009, 80:124-133.
• [38]Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N: Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2004, 2:e69.
• [39]Fallon AM, Baldridge GD, Carroll EM, Kurtz CM: Depletion of host cell riboflavin reduces Wolbachia levels in cultured mosquito cells. In Vitro Cell Dev Biol Anim 2014, 50(8):707-713.
• [40]Darby AC, Armstrong SD, Bah GS, Kaur G, Hughes MA, Kay SM, Koldkjær P, Rainbow L, Radford AD, Blaxter ML: Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 2012, 22:2467-2477.
• [41]Freitak D, Knorr E, Vogel H, Vilcinskas A: Gender- and stressor-specific microRNA expression in Tribolium castaneum. Biol Lett 2012, 8:860-863.
• [42]Rolff J: Bateman's principle and immunity. Proc Biol Sci 2002, 269:867-872.
• [43]Xie RR, Chen XL, Hong XY: Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Appl Entomol Zool 2011, 46:95-102.
• [44]Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD: The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 2008, 6(1):27. BioMed Central Full Text
• [45]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. BioMed Central Full Text
• [46]Wen M, Shen Y, Shi S, Tang T: miREvo: an integrative microRNA evolutionary analysis platform for next-generation sequencing experiments. BMC Bioinformatics 2012, 13:140. BioMed Central Full Text
• [47]Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N: miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res 2012, 40:37-52.
• [48]Zhou L, Chen J, Li ZZ, Li XX, Hu XD, Huang Y, Zhao X, Liang C, Wang Y, Sun L: Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27. 3 associate with clear cell renal cell carcinoma. PLoS One 2010, 5:e15224.
• [49]Robinson MD, Oshlack A: A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 2010, 11:R25. BioMed Central Full Text
• [50]Wang L, Feng Z, Wang X, Wang X, Zhang X: DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010, 26:136-138.
• [51]Storey JD: The positive false discovery rate: A Bayesian interpretation and the q-value. Ann Stat 2003, 31:2013-2035.
• [52]Enright AJ, John B, Gaul U, Tuschl T, Sander C, Marks DS: MicroRNA targets in Drosophila. Genome Biol 2004, 5:R1-R1.
• [53]Young MD, Wakefield MJ, Smyth GK, Oshlack A: Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 2010, 11:R14. BioMed Central Full Text
• [54]Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T: KEGG for linking genomes to life and the environment. Nucleic Acids Res 2008, 36:D480-D484.
• [55]Mao X, Cai T, Olyarchuk JG, Wei L: Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 2005, 21:3787-3793.