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A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility.

Bossan B, Koehncke A, Hammerstein P - PLoS ONE (2011)

Bottom Line: The mistiming-model requires fewer assumptions but has been contradicted by empirical results.Finally, we suggest empirical tests that would allow to distinguish between the models.Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt University, Berlin, Germany. benjamin.bossan@hu-berlin.de

ABSTRACT
Wolbachia are intracellular bacteria transmitted almost exclusively vertically through eggs. In response to this mode of transmission, Wolbachia strategically manipulate their insect hosts' reproduction. In the most common manipulation type, cytoplasmic incompatibility, infected males can only mate with infected females, but infected females can mate with all males. The mechanism of cytoplasmic incompatibility is unknown; theoretical and empirical findings need to converge to broaden our understanding of this phenomenon. For this purpose, two prominent models have been proposed: the mistiming-model and the lock-key-model. The former states that Wolbachia manipulate sperm of infected males to induce a fatal delay of the male pronucleus during the first embryonic division, but that the bacteria can compensate the delay by slowing down mitosis in fertilized eggs. The latter states that Wolbachia deposit damaging "locks" on sperm DNA of infected males, but can also provide matching "keys" in infected eggs to undo the damage. The lock-key-model, however, needs to assume a large number of locks and keys to explain all existing incompatibility patterns. The mistiming-model requires fewer assumptions but has been contradicted by empirical results. We therefore expand the mistiming-model by one quantitative dimension to create the new, so-called goalkeeper-model. Using a method based on formal logic, we show that both lock-key- and goalkeeper-model are consistent with existing data. Compared to the lock-key-model, however, the goalkeeper-model assumes only two factors and provides an idea of the evolutionary emergence of cytoplasmic incompatibility. Available cytological evidence suggests that the hypothesized second factor of the goalkeeper-model may indeed exist. Finally, we suggest empirical tests that would allow to distinguish between the models. Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

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How bidirectionally and unidirectionally incompatible Wolbachia strains are represented in the lock-key-model.(A) strains  and  are bidirectionally incompatible: Neither  nor  has the key to each other's lock. (B)  and  are unidirectionally incompatible:  has the key to 's lock, but  does not have the key to 's lock.
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pone-0019757-g001: How bidirectionally and unidirectionally incompatible Wolbachia strains are represented in the lock-key-model.(A) strains and are bidirectionally incompatible: Neither nor has the key to each other's lock. (B) and are unidirectionally incompatible: has the key to 's lock, but does not have the key to 's lock.

Mentions: According to the analysis by Poinsot et al. [14], the best account for the facts is given by the lock-key-model. In this model, Wolbachia deposit “locks” to the paternal DNA that render these chromosomes unable to participate in mitosis, whereas in the egg cytoplasm, Wolbachia deposit the matching “keys” that recover the functionality of the paternal DNA (Fig. 1). If all locks are matched by corresponding keys, a mating is compatible. By assuming that different strains produce different pairs of locks and keys, bidirectional incompatibility can be explained. The lock-key-model also explains the other known CI patterns. However, molecular evidence for the existence of locks and keys is lacking [14].


A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility.

Bossan B, Koehncke A, Hammerstein P - PLoS ONE (2011)

How bidirectionally and unidirectionally incompatible Wolbachia strains are represented in the lock-key-model.(A) strains  and  are bidirectionally incompatible: Neither  nor  has the key to each other's lock. (B)  and  are unidirectionally incompatible:  has the key to 's lock, but  does not have the key to 's lock.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3091874&req=5

pone-0019757-g001: How bidirectionally and unidirectionally incompatible Wolbachia strains are represented in the lock-key-model.(A) strains and are bidirectionally incompatible: Neither nor has the key to each other's lock. (B) and are unidirectionally incompatible: has the key to 's lock, but does not have the key to 's lock.
Mentions: According to the analysis by Poinsot et al. [14], the best account for the facts is given by the lock-key-model. In this model, Wolbachia deposit “locks” to the paternal DNA that render these chromosomes unable to participate in mitosis, whereas in the egg cytoplasm, Wolbachia deposit the matching “keys” that recover the functionality of the paternal DNA (Fig. 1). If all locks are matched by corresponding keys, a mating is compatible. By assuming that different strains produce different pairs of locks and keys, bidirectional incompatibility can be explained. The lock-key-model also explains the other known CI patterns. However, molecular evidence for the existence of locks and keys is lacking [14].

Bottom Line: The mistiming-model requires fewer assumptions but has been contradicted by empirical results.Finally, we suggest empirical tests that would allow to distinguish between the models.Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

View Article: PubMed Central - PubMed

Affiliation: Institute for Theoretical Biology, Humboldt University, Berlin, Germany. benjamin.bossan@hu-berlin.de

ABSTRACT
Wolbachia are intracellular bacteria transmitted almost exclusively vertically through eggs. In response to this mode of transmission, Wolbachia strategically manipulate their insect hosts' reproduction. In the most common manipulation type, cytoplasmic incompatibility, infected males can only mate with infected females, but infected females can mate with all males. The mechanism of cytoplasmic incompatibility is unknown; theoretical and empirical findings need to converge to broaden our understanding of this phenomenon. For this purpose, two prominent models have been proposed: the mistiming-model and the lock-key-model. The former states that Wolbachia manipulate sperm of infected males to induce a fatal delay of the male pronucleus during the first embryonic division, but that the bacteria can compensate the delay by slowing down mitosis in fertilized eggs. The latter states that Wolbachia deposit damaging "locks" on sperm DNA of infected males, but can also provide matching "keys" in infected eggs to undo the damage. The lock-key-model, however, needs to assume a large number of locks and keys to explain all existing incompatibility patterns. The mistiming-model requires fewer assumptions but has been contradicted by empirical results. We therefore expand the mistiming-model by one quantitative dimension to create the new, so-called goalkeeper-model. Using a method based on formal logic, we show that both lock-key- and goalkeeper-model are consistent with existing data. Compared to the lock-key-model, however, the goalkeeper-model assumes only two factors and provides an idea of the evolutionary emergence of cytoplasmic incompatibility. Available cytological evidence suggests that the hypothesized second factor of the goalkeeper-model may indeed exist. Finally, we suggest empirical tests that would allow to distinguish between the models. Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.

Show MeSH
Related in: MedlinePlus