Sexual transmission of the [Het-s] prion leads to meiotic drive in Podospora anserina

  1. Henk J. P. Dalstra†,‡,
  2. Klaas Swart†,
  3. Alfons J. M. Debets†,
  4. Sven J. Saupe§, and
  5. Rolf F. Hoekstra†
  1. †Laboratory of Genetics, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
  2. §Laboratoire de Génétique Moléculaire des Champignons, Institut de Biochemie et Génétique Cellulaires, Unité Mixte de Recherche 5095, Centre National de la Recherche Scientifique, 33077 Bordeaux, France

  1. Edited by Reed B. Wickner, National Institutes of Health, Bethesda, MD, and approved March 24, 2003 (received for review January 7, 2003)

Abstract

In the filamentous fungus Podospora anserina, two phenomena are associated with polymorphism at the het-s locus, vegetative incompatibility and ascospore abortion. Two het-s alleles occur naturally, het-s and het-S. The het-s encoded protein is a prion propagating as a self-perpetuating amyloid aggregate. When prion-infected [Het-s] hyphae fuse with [Het-S] hyphae, the resulting heterokaryotic cells necrotize. [Het-s] and [Het-S] strains are sexually compatible. When, however, a female [Het-s] crosses with [Het-S], a significant percentage of het-S spores abort, in a way similar to spore killing in Neurospora and Podospora. We report here that sexual transmission of the [Het-s] prion after nonisogamous mating in the reproductive cycle of Podospora is responsible for the killing of het-S spores. Progeny of crosses between isogenic strains with distinct wild-type or introduced, ectopic het-s/S alleles were cytologically and genetically analyzed. The effect of het-s/S overexpression, ectopic het-s/S expression, absence of het-s expression, loss of [Het-s] prion infection, and the distribution patterns of HET-s/S-GFP proteins were categorized during meiosis and ascospore formation. This study unveiled a het-S spore-killing system that is governed by dosage of and interaction between the [Het-s] prion and the HET-S protein. Due to this property of the [Het-s] prion, the het-s allele acts as a meiotic drive element favoring maintenance of the prion-forming allele in natural populations.

Footnotes

  • ↵ ‡ To whom correspondence should be addressed. E-mail: Henk.Dalstra{at}wur.nl.

  • This paper was submitted directly (Track II) to the PNAS office.

  • Abbreviations: het-S, Het-(large)-S allele; het-s, Het-(small)-s allele; het-s0, Het-s0 knockout mutant; HET-S, Het-S protein; HET-s*, Het-s* protein (inactive); HET-s, Het-s prion protein (active); [Het-S], Het-S phenotype; [Het-s*], Het-s* phenotype (noninfected); [Het-s], Het-s phenotype (prion-infected); [Het-s0], Het-s0 knockout phenotype(no HET-s expression); ect-het-S, ectopically integrated het-S gene; ect-het-s, ectopically integrated het-s gene; pGPD-het-S, ectopically integrated het-S gene with a strong GPD promoter; pGPD-het-s, ectopically integrated het-s gene with a GPD promoter; -GFP, fused to GFP; DAPI, 4′,6-diamidino-2-phenylindole.

  • See commentary on page 6292.

  • ↵ The het-s0 knockout mutant was constructed by gene replacement (25) in het-s.

  • ↵ ∥ All ectopic het-s or het-S gene constructs were introduced in a het-s0 strain (11, 23, 17).

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  1. Published online before print April 28, 2003, doi: 10.1073/pnas.1030058100 PNAS May 27, 2003 vol. 100 no. 11 6616-6621
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