Mitochondrial pAL2‐1 plasmid homologs are senescence factors in Podospora anserina independent of intrinsic senescence

Abstract

Since the first description of a linear mitochondrial plasmid in Podospora anserina, pAL2-1, and homologous plasmids have gone from being considered beneficial longevity plasmids, via neutral genetic elements, toward mutator plasmids causing senescence. The plasmid has an invertron structure, with terminal inverted repeats and encodes a DNA and a RNA polymerase. Here we test whether pAL2-1 homologs cause rapid aging independent of intrinsic and external conditions. We first analyzed a natural population of P. anserina and in 40% of the 112 isolates we detected pAL2-1 homologous plasmids. Though the lifespan varied considerably among the strains, plasmid-infected wild-type strains are on average shorter lived than plasmid-free strains and typically show a reduced lifespan extending effect of calorie restriction (CR). However, interesting exceptions were found, inviting further study. To further investigate the effect of pAL2-1 homologs under various conditions, we constructed and analyzed isogenic lines with and without the plasmid. We found that the presence of pAL2-1 homologs did not significantly affect growth rate as suggested by the population analysis, but reduced lifespan under all conditions. This effect was particularly clear for the lifespan extending conditions tested (CR, low temperature, antibiotics) supporting the idea that pAL2-1 homologs are additional senescence factors independent of the intrinsic senescence determinants.

High natural prevalence of a fungal prion

“…The P. anserina laboratory strains were all derived from strain S and have been described (15,42). The natural P. anserina isolates were collected by growing mycelium from fragments of herbivore feces collected on fields around Wageningen, The Netherlands, since 1991 and were stored at −80°C (37,43). Spores were collected from emerging P. anserine-like fruiting bodies.…”

“…Forty percent of our P. anserina isolates were found to be infected with pAL2-1, a mitochondrial senescence plasmid that reduces the lifespan of P. anserina under all conditions tested (37). We combined these data with our het-s genotyping data and found 37 of the 72 het-s isolates and 8 of the 40 het-S isolates carried the plasmid, (Fig.…”

“…Classically, it is proposed that fungal incompatibility systems serve to limit propagation of deleterious cytoplasmic elements such as mycoviruses and senescence plasmids (16)(17)(18). In a previous study, it was found that 40 percent of the P. anserina isolates from the population were infected with the cytoplasmic element pAL2-1, a well-studied mitochondrial senescence plasmid that reduces lifespan (37). If heterokaryon incompatibility restricts plasmid transmission in the wild, it is expected that strains carrying the rarer het allele are less likely to become infected with deleterious cytoplasmic elements.…”

Mitochondrial fusion and inheritance of the mitochondrial genome

“…In the ascomycete Podospora, it has been suggested that strains acquire integrations of a mitochondrial plasmid pAL2-1 into favorable, neutral, or unfavorable locations of the mitochondrial genome, and thus, these strains show variable phenotypes for enhanced or reduced lifespan (van Diepeningen et al 2008). The mF plasmid also recombines with the mitochondrial genome (Fig.…”

Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family

“…We have analysed the size of the WD domain of the het-r locus in a sample of ten natural isolates of P. anserina randomly chosen from a collection already described (van der Gaag et al 2000;van Diepeningen et al 2008) or retrieved from the CBS (Centraal Bureau voor Schimmelcultures, Utrecht, The Netherlands), thereby extending our previous analysis of natural isolates from France ). The number of WD40 repeats was deduced from the size of the WD repeat domain amplicons, and are reported in Table 2.…”