title: Two nuclear life cycle-regulated genes encode interchangeable subunits c of mitochondrial ATP synthase in Podospora anserina.
abstract: An F(1)F(O) ATP synthase in the inner mitochondrial membrane catalyzes the late steps of ATP production via the process of oxidative phosphorylation. A small protein subunit (subunit c or ATP9) of this enzyme shows a substantial genetic diversity, and its gene can be found in both the mitochondrion and/or nucleus. In a representative set of 26 species of fungi for which the genomes have been entirely sequenced, we found five Atp9 gene repartitions. The phylogenetic distribution of nuclear and mitochondrial Atp9 genes suggests that their evolution has included two independent transfers to the nucleus followed by several independent episodes of the loss of the mitochondrial and/or nuclear gene. Interestingly, we found that in Podospora anserina, subunit c is exclusively produced from two nuclear genes (PaAtp9-5 and PaAtp9-7), which display different expression profiles through the life cycle of the fungus. The PaAtp9-5 gene is specifically and strongly expressed in germinating ascospores, whereas PaAtp9-7 is mostly transcribed during sexual reproduction. Consistent with these observations, deletion of PaAtp9-5 is lethal, whereas PaAtp9-7 deletion strongly impairs ascospore production. The P. anserina PaAtp9-5 and PaAtp9-7 genes are therefore nonredundant. By swapping the 5' and 3' flanking regions between genes we demonstrated, however, that the PaAtp9 coding sequences are functionally interchangeable. These findings show that after transfer to the nucleus, the subunit c gene in Podospora became a key target for the modulation of cellular energy metabolism according to the requirements of the life cycle.
authors.affiliation: Univ Paris-Sud, Orsay, France.
authors.forename: Michelle
authors.initials: M
authors.lastname: Déquard-Chablat
authors.forename: Carole H
authors.initials: CH
authors.lastname: Sellem
authors.forename: Pawel
authors.initials: P
authors.lastname: Golik
authors.forename: Frédérique
authors.initials: F
authors.lastname: Bidard
authors.forename: Alexandre
authors.initials: A
authors.lastname: Martos
authors.forename: Maïlis
authors.initials: M
authors.lastname: Bietenhader
authors.forename: Jean-Paul
authors.initials: JP
authors.lastname: di Rago
authors.forename: Annie
authors.initials: A
authors.lastname: Sainsard-Chanet
authors.forename: Sylvie
authors.initials: S
authors.lastname: Hermann-Le Denmat
authors.forename: Véronique
authors.initials: V
authors.lastname: Contamine
mesh_terms: D001483:Base Sequence; D002467:Cell Nucleus; D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism; D017353:Gene Deletion; D018507:Gene Expression Regulation, Developmental; D015966:Gene Expression Regulation, Fungal; D025261:Mitochondrial Proton-Translocating ATPases / Q000235:genetics* / Q000378:metabolism; D008969:Molecular Sequence Data; D025282:Mycelium / Q000235:genetics / Q000254:growth & development; D010641:Phenotype; D010802:Phylogeny; D048468:Podospora / Q000201:enzymology / Q000235:genetics* / Q000254:growth & development; D021122:Protein Subunits; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D020133:Reverse Transcriptase Polymerase Chain Reaction; D016415:Sequence Alignment; D013172:Spores, Fungal / Q000235:genetics / Q000254:growth & development
chemical_list: D005656:Fungal Proteins; D021122:Protein Subunits; D012333:RNA, Messenger; C103607:mitochondrial ATPase subunit c; D025261:Mitochondrial Proton-Translocating ATPases