Unravelling the Wolbachia evolutionary role: The reprogramming of the host genomic imprinting

Ilaria Negri*, Antonella Franchini, Elena Gonella, Daniele Daffonchio, Peter John Mazzoglio, Mauro Mandrioli, Alberto Alma

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

48 Scopus citations

Abstract

Environmental factors can induce significant epigenetic changes that may also be inherited by future generations. The maternally inherited symbiont of arthropods Wolbachia pipientis is an excellent candidate as an 'environmental' factor promoting trans-generational epigenetic changes: by establishing intimate relationships with germ-line cells, epigenetic effects of Wolbachia symbiosis would be manifested as a 'maternal effect', in which infection of the mother modulates the offspring phenotype. In the leafhopper Zyginidia pullula, Wolbachia feminizes genetic males, leaving them as intersexes. With the exception of male chitinous structures that are present in the last abdominal segment, feminized males display phenotypic features that are typical of females. These include ovaries that range from a typical histological architecture to an altered structure. Methylation-sensitive random amplification of polymorphic DNA profiles show that they possess a female genomic imprint. On the other hand, some rare feminized males bear testes instead of ovaries. These specimens possess a Wolbachia density approximately four orders of magnitude lower than feminized males with ovaries and maintain a male genome - methylation pattern. Our results indicate that Wolbachia infection disrupts male imprinting, which dramatically influences the expression of genes involved in sex differentiation and development, and the alteration occurs only if Wolbachia exceeds a density threshold. Thus, a new Wolbachia's role as an environmental evolutionary force, inducing epigenetic trans-generational changes, should now be considered.

Original languageEnglish (US)
Pages (from-to)2485-2491
Number of pages7
JournalProceedings of the Royal Society B: Biological Sciences
Volume276
Issue number1666
DOIs
StatePublished - Jul 7 2009

Keywords

  • Bacterium density
  • DNA methylation
  • Histology
  • Male feminization
  • Wolbachia pipientis
  • Zyginidia pullula

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Immunology and Microbiology(all)
  • Environmental Science(all)
  • Agricultural and Biological Sciences(all)

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