The Endosymbiotic Bacterium Wolbachia Selectively Kills Male Hosts by Targeting the Masculinizing Gene

PLoS Pathogens

Volumn 11, Issue 7, 2015, Pages

  Fukui, Takahiro ^a   Kawamoto, Munetaka ^a   Shoji, Keisuke ^a   Kiuchi, Takashi ^a   Sugano, Sumio ^b   Shimada, Toru ^a   Suzuki, Yutaka ^b   Katsuma, Susumu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; ZINC FINGER PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GENETIC TRANSFECTION; MALE; MASCULINIZING GENE; MOTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WOLBACHIA; ANIMAL; GENETICS; MOLECULAR GENETICS; PARASITOLOGY;

BACTERIA (MICROORGANISMS); BOMBYX MORI; HEXAPODA; LEPIDOPTERA; OSTRINIA; OSTRINIA FURNACALIS; WOLBACHIA;

ANIMALS; FEMALE; MALE; MOLECULAR SEQUENCE DATA; MOTHS; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSFECTION; WOLBACHIA; ZINC FINGERS;

EID: 84938789068     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005048     Document Type: Article

References (24)

1. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH, How many species are infected with Wolbachia?—a statistical analysis of current data. FEMS Microbiol Lett. 2008; 281: 215–220. doi: 10.1111/j.1574-6968.2008.01110.x 18312577
2. Werren JH, Baldo L, Clark ME, Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol. 2008;6: 741–751. doi: 10.1038/nrmicro1969 18794912
3. Fialho RF, Stevens L, Male-killing Wolbachia in a flour beetle. Proc R Soc Lond B. 2000;267: 1469–1473.
4. Dyer KA, Jaenike J, Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 2004;168: 1443–1455. 15579697
5. Kageyama D, Traut W, Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc Biol Sci. 2004;271: 251–258. 15058435
6. Sugimoto TN, Fujii T, Kayukawa T, Sakamoto H, Ishikawa Y, Expression of a doublesex homologue is altered in sexual mosaics of Ostrinia scapulalis moths infected with Wolbachia. Insect Biochem Mol Biol. 2010;40: 847–854. doi: 10.1016/j.ibmb.2010.08.004 20728536
7. Sugimoto TN, Ishikawa Y, A male-killing Wolbachia carries a feminizing factor and is associated with degradation of the sex-determining system of its host. Biol Lett. 2012;8: 412–415. doi: 10.1098/rsbl.2011.1114 22219393
8. Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T, Analysis of the biological functions of a doublesex homologue in Bombyx mori. Dev Genes Evol. 2003;213: 345–354. 12733073
9. Suzuki MG, Funaguma S, Kanda T, Tamura T, Shimada T, Role of the male BmDSX protein in the sexual differentiation of Bombyx mori. Evol Dev. 2005;7: 58–68. 15642090
10. Traut W, Sahara K, Marec F, Sex chromosomes and sex determination in Lepidoptera. Sex Dev. 2007;1: 332–346. doi: 10.1159/000111765 18391545
11. Fujii T, Shimada T, Sex determination in the silkworm, Bombyx mori: a female determinant on the W chromosome and the sex-determining gene cascade. Semin Cell Dev Biol. 2007;18: 379–788. 17446095
12. Hasimoto H, The role of the W-chromosome in the sex determination of Bombyx mori [in Japanese]. Jpn J Genet. 1933;8: 245–247.
13. Tajima Y, Studies on chromosome aberrations in the silkworm. II. Translocation involving second and W-chromosomes [in Japanese]. Bull Seric Exp Stn. 1944;12: 109–181.
14. Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, et al. A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 2014;509: 633–636. doi: 10.1038/nature13315 24828047
15. Kawamoto M, Koga H, Kiuchi T, Shoji K, Sugano S, Shimada T, et al. Sexually biased transcripts at early embryonic stages of the silkworm depend on the sex chromosome constitution. Gene 2015;560: 50–56. doi: 10.1016/j.gene.2015.01.036 25615878
16. Suzuki MG, Imanishi S, Dohmae N, Asanuma M, Matsumoto S, Identification of a male-specific RNA binding protein that regulates sex-specific splicing of Bmdsx by increasing RNA binding activity of BmPSI. Mol Cell Biol. 2010;30: 5776–5786. doi: 10.1128/MCB.00444-10 20956562
17. Penalva LO, Sa´nchez L, RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation. Microbiol Mol Biol Rev. 2003;67: 343–359. 12966139
18. Veneti Z, Bentley JK, Koana T, Braig HR, Hurst GD. A functional dosage compensation complex required for male killing in Drosophila. 2005;307: 1461–1463.
19. Katsuma S, Kawamoto M, Kiuchi T, Guardian small RNAs and sex determination. RNA Biol. 2014;11: 1238–1242. doi: 10.1080/15476286.2014.996060 25588029
20. Kern P, Cook JM, Kageyama D, Riegler M, Double trouble: combined action of meiotic drive and Wolbachia feminization in Eurema butterflies. Biol. Lett. 2015;11: 20150095. doi: 10.1098/rsbl.2015.0095 25948567
21. Sato Y, Yoshizato T, Shiraishi Y, Maekawa S, Okuno Y, Kamura T, et al. Integrated molecular analysis of clear-cell renal cell carcinoma. Nature Genet. 2013;45: 860–867. doi: 10.1038/ng.2699 23797736
22. d'Alençon E, Sezutsu H, Legeai F, Permal E, Bernard-Samain S, Gimenez S, et al. Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements. Proc Natl Acad Sci U S A. 2010;107: 7680–7685. doi: 10.1073/pnas.0910413107 20388903
23. Sahara K, Yoshido A, Shibata F, Fujikawa-Kojima N, Okabe T, Tanaka-Okuyama M, et al. FISH identification of Helicoverpa armigera and Mamestra brassicae chromosomes by BAC and fosmid probes. Insect Biochem Mol Biol. 2013;43: 644–653. doi: 10.1016/j.ibmb.2013.04.003 23628856
24. Kroemer JA, Coates BS, Nusawardani T, Rider SD, JrFraser LM, Hellmich RL, A rearrangement of the Z chromosome topology influences the sex-linked gene display in the European corn borer, Ostrinia nubilalis. Mol Genet Genomics. 2011;286: 37–56. doi: 10.1007/s00438-011-0624-1 21573787