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Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner.

Asgharian H, Chang PL, Mazzoglio PJ, Negri I - Front Microbiol (2014)

Bottom Line: Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories.The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect.Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular and Computational Biology, Department of Biological Sciences, University of Southern California Los Angeles, CA, USA.

ABSTRACT
Wolbachia causes the feminization of chromosomally male embryos in several species of crustaceans and insects, including the leafhopper Zyginidia pullula. In contrast to the relatively well-established ecological aspects of male feminization (e.g., sex ratio distortion and its consequences), the underlying molecular mechanisms remain understudied and unclear. We embarked on an exploratory study to investigate the extent and nature of Wolbachia's effect on gene expression pattern in Z. pullula. We sequenced whole transcriptomes from Wolbachia-infected and uninfected adults. 18147 loci were assembled de novo, including homologs of several Drosophila sex determination genes. A number of transcripts were flagged as candidate Wolbachia sequences. Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories. The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect. Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

No MeSH data available.


Related in: MedlinePlus

Sex determination pathway in Drosophila, modified from Sánchez (2008). SxlF and SxlM refer to functional female and nonfunctional male isoforms of the Sxl protein, respectively. TraF is the functional female form of the Transformer protein, which in conjunction with the constitutive gene product Tra-2 controls female-specific splicing of dsx and fru. snf, vir and FL(2)D are required for late female-specific splicing of Sxl but play no part in determining early Sxl splicing pattern. The genes for which Z. pullula homologs have been identified in this study, are boxed in gray. For more details on the regulation and function of these genes, refer to (Sánchez, 2008; Gempe and Beye, 2011) or other similar resources. Reproduced with permission from The International Journal of Developmental Biology (Int. J. Dev. Biol.) (2008) Vol:52, pp. 837–856.
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Figure 1: Sex determination pathway in Drosophila, modified from Sánchez (2008). SxlF and SxlM refer to functional female and nonfunctional male isoforms of the Sxl protein, respectively. TraF is the functional female form of the Transformer protein, which in conjunction with the constitutive gene product Tra-2 controls female-specific splicing of dsx and fru. snf, vir and FL(2)D are required for late female-specific splicing of Sxl but play no part in determining early Sxl splicing pattern. The genes for which Z. pullula homologs have been identified in this study, are boxed in gray. For more details on the regulation and function of these genes, refer to (Sánchez, 2008; Gempe and Beye, 2011) or other similar resources. Reproduced with permission from The International Journal of Developmental Biology (Int. J. Dev. Biol.) (2008) Vol:52, pp. 837–856.

Mentions: A number of genes potentially involved in the leafhopper sex determination were identified through homology search with the Drosophila sex determination genes. Although pea aphid is Zyginidia's closest relative with a reference genome sequence (The International Aphid Genomics Consortium, 2010), the functional annotation for this genome is not as complete as that of Drosophila. Sex determining genes of pea aphid have been found based on homology with Drosophila sequences and lack direct experimental verification (The International Aphid Genomics Consortium, 2010). Therefore, we decided to use Drosophila sequences as the reference set. Figure 1 depicts the canonical sex determination pathway in Drosophila. Homologs of several Drosophila sex determination genes were identified among the transcripts including dsx (doublesex), tra-2 (transformer-2), vir (virilizer), fl(2)d (female lethal d), snf (sans fille) and ix (intersex). No leafhopper homologs could be identified for tra (transformer), sxl (sex lethal), fru (fruitless) or her (hermaphrodite). Table 2 shows the expression levels for the identified leafhopper sex determination genes.


Wolbachia is not all about sex: male-feminizing Wolbachia alters the leafhopper Zyginidia pullula transcriptome in a mainly sex-independent manner.

Asgharian H, Chang PL, Mazzoglio PJ, Negri I - Front Microbiol (2014)

Sex determination pathway in Drosophila, modified from Sánchez (2008). SxlF and SxlM refer to functional female and nonfunctional male isoforms of the Sxl protein, respectively. TraF is the functional female form of the Transformer protein, which in conjunction with the constitutive gene product Tra-2 controls female-specific splicing of dsx and fru. snf, vir and FL(2)D are required for late female-specific splicing of Sxl but play no part in determining early Sxl splicing pattern. The genes for which Z. pullula homologs have been identified in this study, are boxed in gray. For more details on the regulation and function of these genes, refer to (Sánchez, 2008; Gempe and Beye, 2011) or other similar resources. Reproduced with permission from The International Journal of Developmental Biology (Int. J. Dev. Biol.) (2008) Vol:52, pp. 837–856.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150536&req=5

Figure 1: Sex determination pathway in Drosophila, modified from Sánchez (2008). SxlF and SxlM refer to functional female and nonfunctional male isoforms of the Sxl protein, respectively. TraF is the functional female form of the Transformer protein, which in conjunction with the constitutive gene product Tra-2 controls female-specific splicing of dsx and fru. snf, vir and FL(2)D are required for late female-specific splicing of Sxl but play no part in determining early Sxl splicing pattern. The genes for which Z. pullula homologs have been identified in this study, are boxed in gray. For more details on the regulation and function of these genes, refer to (Sánchez, 2008; Gempe and Beye, 2011) or other similar resources. Reproduced with permission from The International Journal of Developmental Biology (Int. J. Dev. Biol.) (2008) Vol:52, pp. 837–856.
Mentions: A number of genes potentially involved in the leafhopper sex determination were identified through homology search with the Drosophila sex determination genes. Although pea aphid is Zyginidia's closest relative with a reference genome sequence (The International Aphid Genomics Consortium, 2010), the functional annotation for this genome is not as complete as that of Drosophila. Sex determining genes of pea aphid have been found based on homology with Drosophila sequences and lack direct experimental verification (The International Aphid Genomics Consortium, 2010). Therefore, we decided to use Drosophila sequences as the reference set. Figure 1 depicts the canonical sex determination pathway in Drosophila. Homologs of several Drosophila sex determination genes were identified among the transcripts including dsx (doublesex), tra-2 (transformer-2), vir (virilizer), fl(2)d (female lethal d), snf (sans fille) and ix (intersex). No leafhopper homologs could be identified for tra (transformer), sxl (sex lethal), fru (fruitless) or her (hermaphrodite). Table 2 shows the expression levels for the identified leafhopper sex determination genes.

Bottom Line: Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories.The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect.Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular and Computational Biology, Department of Biological Sciences, University of Southern California Los Angeles, CA, USA.

ABSTRACT
Wolbachia causes the feminization of chromosomally male embryos in several species of crustaceans and insects, including the leafhopper Zyginidia pullula. In contrast to the relatively well-established ecological aspects of male feminization (e.g., sex ratio distortion and its consequences), the underlying molecular mechanisms remain understudied and unclear. We embarked on an exploratory study to investigate the extent and nature of Wolbachia's effect on gene expression pattern in Z. pullula. We sequenced whole transcriptomes from Wolbachia-infected and uninfected adults. 18147 loci were assembled de novo, including homologs of several Drosophila sex determination genes. A number of transcripts were flagged as candidate Wolbachia sequences. Despite the resemblance of Wolbachia-infected chromosomal males to uninfected and infected chromosomal females in terms of sexual morphology and behavior, principal component analysis revealed that gene expression patterns did not follow these sexual phenotype categories. The principal components generated by differentially expressed genes specified a strong sex-independent Wolbachia effect, followed by a weaker Wolbachia-sexual karyotype interaction effect. Approaches to further examine the molecular mechanism of Wolbachia-host interactions have been suggested based on the presented findings.

No MeSH data available.


Related in: MedlinePlus