TY - JOUR
T1 - The Wolbachia protein TomO interacts with a host RNA to induce polarization defects in Drosophila oocytes
AU - Ote, Manabu
AU - Yamamoto, Daisuke
N1 - Funding Information:
We thank Akira Nakamura for anti-Cup antibodies and Azusa Utsumi for secretarial assistance. This work was supported, in part, by Grants-in-Aid for Scientific Research (nos. 17K19371, 17H05935, and 16H06371) from MEXT to D.Y.
Publisher Copyright:
© 2018 Wiley Periodicals, Inc.
PY - 2018/9
Y1 - 2018/9
N2 - Wolbachia is an endosymbiont prevalent in arthropods. To maximize its transmission thorough the female germline, Wolbachia induces in infected hosts male-to-female transformation, male killing, parthenogenesis, and cytoplasmic incompatibility, depending on the host species and Wolbachia strain involved. However, the molecular mechanisms underlying these host manipulations by Wolbachia remain largely unknown. The Wolbachia strain wMel, an inhabitant of Drosophila melanogaster, impairs host oogenesis only when transplanted into a heterologous host, for example, Drosophila simulans. We found that egg polarity defects induced by wMel infection in D. simulans can be recapitulated in the natural host D. melanogaster by transgenic overexpression of a variant of the Wolbachia protein Toxic manipulator of oogenesis (TomO), TomOw Mel ∆HS, in the female germline. RNA immunoprecipitation assays demonstrated that TomO physically associates with orb mRNA, which, as a result, fails to interact with the translation repressor Cup. This leads to precocious translation of Orb, a posterior determinant, and thereby to the misspecification of oocytes and accompanying polarity defects. We propose that the ability of TomO to bind to orb mRNA might provide a means for Wolbachia to enter the oocyte located at the posterior end of the egg chamber, thereby accomplishing secure maternal transmission thorough the female germline.
AB - Wolbachia is an endosymbiont prevalent in arthropods. To maximize its transmission thorough the female germline, Wolbachia induces in infected hosts male-to-female transformation, male killing, parthenogenesis, and cytoplasmic incompatibility, depending on the host species and Wolbachia strain involved. However, the molecular mechanisms underlying these host manipulations by Wolbachia remain largely unknown. The Wolbachia strain wMel, an inhabitant of Drosophila melanogaster, impairs host oogenesis only when transplanted into a heterologous host, for example, Drosophila simulans. We found that egg polarity defects induced by wMel infection in D. simulans can be recapitulated in the natural host D. melanogaster by transgenic overexpression of a variant of the Wolbachia protein Toxic manipulator of oogenesis (TomO), TomOw Mel ∆HS, in the female germline. RNA immunoprecipitation assays demonstrated that TomO physically associates with orb mRNA, which, as a result, fails to interact with the translation repressor Cup. This leads to precocious translation of Orb, a posterior determinant, and thereby to the misspecification of oocytes and accompanying polarity defects. We propose that the ability of TomO to bind to orb mRNA might provide a means for Wolbachia to enter the oocyte located at the posterior end of the egg chamber, thereby accomplishing secure maternal transmission thorough the female germline.
KW - Drosophila
KW - TomO
KW - Wolbachia
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U2 - 10.1002/arch.21475
DO - 10.1002/arch.21475
M3 - Article
AN - SCOPUS:85047805483
VL - 99
JO - Archives of Insect Biochemistry and Physiology
JF - Archives of Insect Biochemistry and Physiology
SN - 0739-4462
IS - 1
M1 - e21475
ER -