Academic journal article Genetics

Multiple Rescue Factors within a Wolbachia Strain

Academic journal article Genetics

Multiple Rescue Factors within a Wolbachia Strain

Article excerpt

ABSTRACT

Wolbachia-induced cytoplasmic incompatibility (CI) is expressed when infected males are crossed with either uninfected females or females infected with Wolbachia of different CI specificity. In diploid insects, CI results in embryonic mortality, apparently due to the the loss of the paternal set of chromosomes, usually during the first mitotic division. The molecular basis of CI has not been determined yet; however, several lines of evidence suggest that Wolbachia exhibits two distinct sex-dependent functions: in males, Wolbachia somehow "imprints" the paternal chromosomes during spermatogenesis (mod function), whereas in females, the presence of the same Wolbachia strain(s) is able to restore embryonic viability (resc function). On the basis of the ability of Wolbachia to induce the modification and/or rescue functions in a given host, each bacterial strain can be classified as belonging in one of the four following categories: mod^sup +^ resc^sup +^, mod^sup -^ resc^sup +^, mod^sup -^ resc^sup -^, and mod^sup +^ resc^sup -^. A so-called "suicide" mod^sup +^ resc^sup -^ strain has not been found in nature yet. Here, a combination of embryonic cytoplasmic injections and introgression experiments was used to transfer nine evolutionary, distantly related Wolbachia strains (wYak, wTei, wSan, wRi, wMel, wHa, wAu, wNo, and wMa) into the same host background, that of Drosophila simulans (STCP strain), a highly permissive host for CI expression. We initially characterized the modification and rescue properties of the Wolbachia strains wYak, wTei, and wSan, naturally present in the yakuba complex, upon their transfer into D. simulans. Confocal microscopy and multilocus sequencing typing (MLST) analysis were also employed for the evaluation of the CI properties. We also tested the compatibility relationships of wYak, wTei, and wSan with all other Wolbachia infections. So far, the cytoplasmic incompatibility properties of different Wolbachia variants are explained assuming a single pair of modification and rescue factors specific to each variant. This study shows that a given Wolbachia variant can possess multiple rescue determinants corresponding to different CI systems. In addition, our results: (a) suggest that wTei appears to behave in D. simulans as a suicide mod^sup +^ resc^sup -^ strain, (b) unravel unique CI properties, and (c) provide a framework to understand the diversity and the evolution of new CI-compatibility types.

WOLBACHIA is a group of maternally transmitted intracellular bacteria that infect numerous arthropod as well as filarial nematode species (Werren 1997; Bandi et al. 1998; Stouthamer et al. 1999). In arthropod hosts, Wolbachia mainly reside in ovaries and testes. In many cases, they manipulate host reproduction to ensure their own transmission by inducing feminization (Rigaud 1997), thelytokous parthenogenesis (Huigens and Stouthamer 2003), male killing (Hurst et al. 2003) and, most commonly, cytoplasmic incompatibility (CI) (Bourtzis et al. 2003). In diploid species, CI is expressed as embryonic lethality of the progeny of a male infected by one (or more) Wolbachia strain(s) and a female that either is uninfected or carries a different Wolbachia strain (Bourtzis et al. 2003).

The molecular mechanism of CI has not yet been elucidated; currently available data, however, suggest that Wolbachia modifies nuclear components of the spermduring spermatogenesis (Presgraves 2000). This is called the modification action of Wolbachia (mod function) (Werren 1997). This modification prevents the paternal set of chromosomes from entering the anaphase of the first mitotic division, resulting in failure of zygote development unless the sameWolbachia strain(s) is/are present in the egg and exert(s) the respective rescue function(s) (resc, for rescue) (Lassy and Karr 1996; Callaini et al. 1997; Werren 1997; Tram and Sullivan 2002; Ferree and Sullivan 2006). It has been suggested that mod and resc interact in a lock-and-key manner, with a direct inhibition of the mod factor (the lock) by the resc factor (the key) (Poinsot et al. …

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