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Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi.

Publication ,  Journal Article
Wang, X; Hsueh, Y-P; Li, W; Floyd, A; Skalsky, R; Heitman, J
Published in: Genes Dev
November 15, 2010

Cosuppression is a silencing phenomenon triggered by the introduction of homologous DNA sequences into the genomes of organisms as diverse as plants, fungi, flies, and nematodes. Here we report sex-induced silencing (SIS), which is triggered by tandem integration of a transgene array in the human fungal pathogen Cryptococcus neoformans. A SXI2a-URA5 transgene array was found to be post-transcriptionally silenced during sexual reproduction. More than half of the progeny that inherited the SXI2a-URA5 transgene became uracil-auxotrophic due to silencing of the URA5 gene. In vegetative mitotic growth, silencing of this transgene array occurred at an ∼250-fold lower frequency, indicating that silencing is induced during the sexual cycle. Central components of the RNAi pathway-including genes encoding Argonaute, Dicer, and an RNA-dependent RNA polymerase-are all required for both meiotic and mitotic transgene silencing. URA5-derived ∼22-nucleotide (nt) small RNAs accumulated in the silenced isolates, suggesting that SIS is mediated by RNAi via sequence-specific small RNAs. Through deep sequencing of the small RNA population in C. neoformans, we also identified abundant small RNAs mapping to repetitive transposable elements, and these small RNAs were absent in rdp1 mutant strains. Furthermore, a group of retrotransposons was highly expressed during mating of rdp1 mutant strains, and an increased transposition/mutation rate was detected in their progeny, indicating that the RNAi pathway squelches transposon activity during the sexual cycle. Interestingly, Ago1, Dcr1, Dcr2, and Rdp1 are translationally induced in mating cells, and Ago1, Dcr1, and Dcr2 localize to processing bodies (P bodies), whereas Rdp1 appears to be nuclear, providing mechanistic insights into the elevated silencing efficiency during sexual reproduction. We hypothesize that the SIS RNAi pathway operates to defend the genome during sexual development.

Duke Scholars

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Published In

Genes Dev

DOI

EISSN

1549-5477

Publication Date

November 15, 2010

Volume

24

Issue

22

Start / End Page

2566 / 2582

Location

United States

Related Subject Headings

  • Sex Factors
  • Retroelements
  • Reproduction
  • RNA Interference
  • Genome, Fungal
  • Genes, Fungal
  • Developmental Biology
  • Cryptococcus neoformans
  • Alleles
  • Adenosine Triphosphatases
 

Citation

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Wang, X., Hsueh, Y.-P., Li, W., Floyd, A., Skalsky, R., & Heitman, J. (2010). Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev, 24(22), 2566–2582. https://doi.org/10.1101/gad.1970910
Wang, Xuying, Yen-Ping Hsueh, Wenjun Li, Anna Floyd, Rebecca Skalsky, and Joseph Heitman. “Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi.Genes Dev 24, no. 22 (November 15, 2010): 2566–82. https://doi.org/10.1101/gad.1970910.
Wang X, Hsueh Y-P, Li W, Floyd A, Skalsky R, Heitman J. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev. 2010 Nov 15;24(22):2566–82.
Wang, Xuying, et al. “Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi.Genes Dev, vol. 24, no. 22, Nov. 2010, pp. 2566–82. Pubmed, doi:10.1101/gad.1970910.
Wang X, Hsueh Y-P, Li W, Floyd A, Skalsky R, Heitman J. Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev. 2010 Nov 15;24(22):2566–2582.

Published In

Genes Dev

DOI

EISSN

1549-5477

Publication Date

November 15, 2010

Volume

24

Issue

22

Start / End Page

2566 / 2582

Location

United States

Related Subject Headings

  • Sex Factors
  • Retroelements
  • Reproduction
  • RNA Interference
  • Genome, Fungal
  • Genes, Fungal
  • Developmental Biology
  • Cryptococcus neoformans
  • Alleles
  • Adenosine Triphosphatases