Wolbachia-Mediated Cytoplasmic Incompatibility Is Associated with Impaired Histone Deposition in the Male Pronucleus

Frédéric Landmann,William Sullivan,Guillermo A Orsi,Benjamin Loppin,David S Schneider

doi:10.1371/journal.ppat.1000343

Abstract

Wolbachia is a bacteria endosymbiont that rapidly infects insect populations through a mechanism known as cytoplasmic incompatibility (CI). In CI, crosses between Wolbachia-infected males and uninfected females produce severe cell cycle defects in the male pronucleus resulting in early embryonic lethality. In contrast, viable progeny are produced when both parents are infected (the Rescue cross). An important consequence of CI–Rescue is that infected females have a selective advantage over uninfected females facilitating the rapid spread of Wolbachia through insect populations. CI disrupts a number of prophase and metaphase events in the male pronucleus, including Cdk1 activation, chromosome condensation, and segregation. Here, we demonstrate that CI disrupts earlier interphase cell cycle events. Specifically, CI delays the H3.3 and H4 deposition that occurs immediately after protamine removal from the male pronucleus. In addition, we find prolonged retention of the replication factor PCNA in the male pronucleus into metaphase, indicating progression into mitosis with incompletely replicated DNA. We propose that these CI-induced interphase defects in de novo nucleosome assembly and replication are the cause of the observed mitotic condensation and segregation defects. In addition, these interphase chromosome defects likely activate S-phase checkpoints, accounting for the previously described delays in Cdk1 activation. These results have important implications for the mechanism of Rescue and other Wolbachia-induced phenotypes.

Highlights

Wolbachia are intracellular bacteria that infect some 65% of all insect species [1]
Wolbachia are among the most successful of all intracellular bacteria, infecting an estimated 65% of insect species
Wolbachia’s success is due in part to its ability to induce a conditional form of sterility known as cytoplasmic incompatibility (CI), endowing infected females with a tremendous selective advantage

Summary

Introduction

Wolbachia are intracellular bacteria that infect some 65% of all insect species [1]. Their success is in large part due to their efficient maternal transmission and their ability to alter host reproduction such that infected females produce more offspring than uninfected females [2]. The most common form of altered reproduction is known as cytoplasmic incompatibility (CI), a form of conditional sterility resulting from crosses of Wolbachia-infected males to uninfected females [3]. These crosses produce defects in the first zygotic mitosis resulting in inviable embryos. Infected females enjoy a tremendous selective advantage over uninfected females resulting in the rapid spread of Wolbachia via the maternal lineage [5] The success of this strategy is underscored by the fact that CI has been documented in every insect order [3]

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