Paternal Grandmother Age Affects the Strength of
            <i>Wolbachia</i>
            -Induced Cytoplasmic Incompatibility in Drosophila melanogaster

Layton, Emily M.; On, Jungmin; Perlmutter, Jessamyn I.; Bordenstein, Seth R.; Shropshire, J. Dylan

doi:10.1128/mbio.01879-19

Cited by 43 publications

(68 citation statements)

References 80 publications

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“…Notably, most of the genes were tested singly, and it is possible that they work together to induce a phenotype. Further, Wolbachia strains can induce weak versus strong phenotypes (56,57) or CI versus male killing (11,12), depending on different factors, including host background. Thus, testing candidate genes in other host genetic backgrounds will be an important future direction that may yield new or different results.…”

Section: Discussionmentioning

confidence: 99%

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

2020

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Endosymbiotic bacteria in the genus Wolbachia remarkably infect nearly half of all arthropod species. They spread in part because of manipulations of host sexual reproduction that enhance the maternal transmission of the bacteria, including male killing (death of infected males) and unidirectional cytoplasmic incompatibility (CI; death of offspring from infected fathers and uninfected mothers). Recent discoveries identified several genes in prophage WO of Wolbachia (wmk, cifA, and cifB) that fully or partially recapitulate male killing or CI when transgenically expressed in Drosophila melanogaster. However, it is not yet fully resolved if other gene candidates contribute to these phenotypes. Here, we transgenically tested 10 additional gene candidates for their involvement in male killing and/or CI. The results show that despite sequence and protein architecture similarities or comparative associations with reproductive parasitism, transgenic expression of the candidates does not recapitulate male killing or CI. Sequence analysis across Wmk and its closest relatives reveals amino acids that may be important to its function. In addition, evidence is presented to propose new hypotheses regarding the relationship between wmk transcript length and its ability to kill a given host, as well as copy number of wmk homologs within a bacterial strain, which may be predictive of host resistance. Together, these analyses continue to build the evidence for identification of wmk, cifA, and cifB as the major genes that have thus far been shown to cause reproductive parasitism in Wolbachia, and the transgenic resources provide a basis for further functional study of phage WO genes. IMPORTANCE Wolbachia are widespread bacterial endosymbionts that manipulate the reproduction of diverse arthropods to spread through a population and can substantially shape host evolution. Recently, reports identified three prophage WO genes (wmk, cifA, and cifB) that transgenically recapitulate many aspects of reproductive manipulation in Drosophila melanogaster. Here, we transgenically tested 10 additional gene candidates for CI and/or male killing in flies. The results yield no evidence for the involvement of these gene candidates in reproductive parasitism, bolstering the evidence for identification of the cif and wmk genes as the major factors involved in their phenotypes. In addition, evidence supports new hypotheses for prediction of male-killing phenotypes or lack thereof based on wmk transcript length and copy number. These experiments inform efforts to understand the full basis of reproductive parasitism for basic and applied purposes and lay the foundation for future work on the function of an interesting group of Wolbachia and phage WO genes.

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Section: Discussionmentioning

confidence: 99%

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

2020

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“…CI was measured using hatch rate assays. To control for the paternal grandmother age effect on CI [39], virgin nos-GAL4:VP16 females were collected for the first 3 days of emergence and aged 9-11 days before crossing to nonvirgin UAS transgenic males. Collections for maternal and paternal lineages were separated by a 7-day period.…”

Section: Measurement Assaysmentioning

confidence: 99%

Evolution-guided mutagenesis of the cytoplasmic incompatibility proteins: Identifying CifA’s complex functional repertoire and new essential regions in CifB

2020

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Wolbachia are the world's most common, maternally-inherited, arthropod endosymbionts. Their worldwide distribution is due, in part, to a selfish drive system termed cytoplasmic incompatibility (CI) that confers a relative fitness advantage to females that transmit Wolbachia to their offspring. CI results in embryonic death when infected males mate with uninfected females but not infected females. Under the Two-by-One genetic model of CI, males expressing the two phage WO proteins CifA and CifB cause CI, and females expressing CifA rescue CI. While each protein is predicted to harbor three functional domains, there is no knowledge on how sites across these Cif domains, rather than in any one particular domain, contribute to CI and rescue. Here, we use evolution-guided, substitution mutagenesis of conserved amino acids across the Cif proteins, coupled with transgenic expression in uninfected Drosophila melanogaster, to determine the functional impacts of conserved residues evolving mostly under purifying selection. We report that amino acids in CifA's N-terminal unannotated region and annotated catalase-related domain are important for both complete CI and rescue, whereas C-terminal residues in CifA's putative domain of unknown function are solely important for CI. Moreover, conserved CifB amino acids in the predicted nucleases, peptidase, and unannotated regions are essential for CI. Taken together, these findings indicate that (i) all CifA amino acids determined to be crucial in rescue are correspondingly crucial in CI, (ii) an additional set of CifA amino acids are uniquely important in CI, and (iii) CifB amino acids across the protein, rather than in one particular domain, are all crucial for CI. We discuss how these findings advance an expanded view of Cif protein evolution and function, inform the mechanistic and biochemical bases of Cif-induced CI/rescue, and continue to substantiate the Two-by-One genetic model of CI.

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“…Similarly, heat shock also negatively impacts X-type-mediated survival against A. ervi wasps in the pea aphid (Heyworth & Ferrari 2016). Another possibility, raised by studies of the strength of CI and male-killing exhibited by Wolbachia, is that protection strength is influenced by parental Spiroplasma titre (Dyer et al 2005;Layton et al 2019). It is notable that both thermal environment and age at reproduction are known to affect S. poulsonii titre and male-killing strength in D. melanogaster (Anbutsu & Fukatsu 2003;Montenegro & Klaczko 2004;Anbutsu et al 2008).…”

Section: Discussionmentioning

confidence: 99%

Symbiont-mediated fly survival is independent of defensive symbiont genotype in the Drosophila melanogaster-Spiroplasma-wasp interaction

Jones

Hurst

2020

Preprint

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AbstractWhen a parasite attacks an insect, the outcome is commonly modulated by the presence of defensive heritable symbionts residing within the insect host. Previous studies noted markedly different strengths of Spiroplasma-mediated fly survival following attack by the same strain of wasp. One difference between the two studies was the strain of Spiroplasma used. We therefore performed a common garden laboratory experiment to assess whether Spiroplasma-mediated protection depends upon the strain of Spiroplasma. We perform this analysis using the two strains of male-killing Spiroplasma used previously, and examined response to challenge by two strains of Leptopilina boulardi and two strains of Leptopilina heterotoma wasp. We found no evidence Spiroplasma strain affected fly survival following wasp attack. In contrast, analysis of the overall level of protection, including the fecundity of survivors of wasp attack, did indicate the two Spiroplasma strains tested varied in protective efficiency against three of the four wasp strains tested. These data highlight the sensitivity of symbiont-mediated protection phenotypes to laboratory conditions, and the importance of common garden comparison. Our results also indicate that Spiroplasma strains can vary in protective capacity in Drosophila, but these differences may exist in the relative performance of survivors of wasp attack, rather than in survival of attack per se.

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Paternal Grandmother Age Affects the Strength of Wolbachia -Induced Cytoplasmic Incompatibility in Drosophila melanogaster

Cited by 43 publications

References 80 publications

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

Evolution-guided mutagenesis of the cytoplasmic incompatibility proteins: Identifying CifA’s complex functional repertoire and new essential regions in CifB

Symbiont-mediated fly survival is independent of defensive symbiont genotype in the Drosophila melanogaster-Spiroplasma-wasp interaction

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