Pentatricopeptide repeat 336 as the candidate gene for paternal sorting of mitochondria (Psm) in cucumber.

KEY MESSAGE: Pentatricopeptide repeat (PPR) 336 was identified as the candidate gene for Paternal Sorting of Mitochondria ( Psm ), a nuclear locus that affects the predominant mitochondria transmitted to progenies. Cucumber (Cucumis sativus L.) is a useful plant to study organellar-nuclear interactions because its organelles show differential transmission, maternal for chloroplasts and paternal for mitochondria. The mitochondrial DNA (mtDNA) of cucumber is relatively large due in part to accumulation of repetitive DNAs and recombination among these repetitive regions produces structurally polymorphic mtDNAs associated with paternally transmitted mosaic (MSC) phenotypes. The mitochondrial mutant MSC16 possesses an under-representation of ribosomal protein S7 (rps7), a key component of the small ribosomal subunit in the mitochondrion. A nuclear locus, Paternal Sorting of Mitochondria (Psm), affects the predominant mitochondria transmitted to progenies generated from crosses with MSC16 as the male parent. Using single nucleotide polymorphisms, Psm was mapped to a 170 kb region on chromosome 3 of cucumber and pentatricopeptide repeat (PPR) 336 was identified as the likely candidate gene. PPR336 stabilizes mitochondrial ribosomes in Arabidopsis thaliana and because MSC16 shows reduced transcription of rps7, the cucumber homolog of PPR336 (CsPPR336) as the candidate for Psm is consistent with a nuclear effect on ribosome assembly or stability in the mitochondrion. We used polymorphisms in CsPPR336 to genotype progenies segregating at Psm and recovered only one Psm -/- plant with the MSC phenotype, indicating that the combination of the Psm- allele with mitochondria from MSC16 is almost always lethal. This research illustrates the usefulness of the MSC mutants of cucumber to reveal and study unique interactions between the mitochondrion and nucleus.