Integration of mitochondrial gene sequences within the nuclear genome during senescence in a fungus

Abstract

Cellular senescence in the ascomycete fungus Podospora anserina is associated with the appearance of an altered mitochondrial genome. Discrete mitochondrial DNA sequences are excised and amplified and isolated as multimerically arranged, head-to-tail repetitions. We have referred to the most frequently observed excision/amplification product as alpha-event senDNA. It is a 2.6-kilobase pair (kbp) monomeric unit (see refs 1, 3, 7) and is often found in senescent mitochondria in conjunction with other excision products. At the final stage of senescence these plasmids constitute virtually all of the DNA present in senescent mitochondria; they have replicated to high copy number at the expense of the young native genome. Because P. anserina is characterized by race-specific timing of senescence (that is, a programme of senescence), we have begun to contrast rapidly and slowly senescing races in terms of senDNA. Here we present evidence that young mitochondria of the rapidly senescing race, A+, possess an extremely high copy number of alpha-event senDNA plasmid in contrast to the more slowly senescing races s+ or s-. Moreover, we observe that during senescence the alpha-event senDNA and the beta-event senDNA (a 9.8-kbp monomer) are transposed to the nucleus and integrated into nuclear DNA. These plasmids contain the coding information for subunits I and III (respectively) of the mitochondrial cytochrome c oxidase. This constitutes the first clear evidence for the active mobilization of genetic elements from the mitochondrion to the nucleus.