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

Authors: DEL VALLE-ECHEVARRIA, A - University Of Wisconsin; SANSEVERINO, W - University Of Barcelona; GARCIA-MAS, J - University Of Barcelona; Havey, Michael

Submitted to: Theoretical and Applied Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/2/2016
Publication Date: 7/16/2016
Publication URL: http://handle.nal.usda.gov/10113/5555512
Citation: Del Valle-Echevarria, A.R., Sanseverino, W., Garcia-Mas, J., Havey, M.J. 2016. Pentatricopeptide repeat 336 as the candidate gene for paternal sorting of mitochondria (Psm) in cucumber. Theoretical and Applied Genetics. 129(10):1951-1959. doi: 10.1007/s00122-016-2751-x.

Interpretive Summary: Cucumber is a useful plant to study organellar-nuclear interactions because its three genomes show differential transmission: bi-parental nuclear, maternal chloroplast and paternal mitochondrial (mt). The mt DNA of cucumber is relatively large due in part to accumulation of repetitive DNAs. Recombination among these repetitive regions produces structurally polymorphic mt DNAs associated with paternally transmitted, strongly mosaic (MSC) phenotypes. Mitochondrial mutant MSC16 possesses an under-representation of the rps7 gene, which encodes ribosomal protein S7 crucial for assembly 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 next-generation sequencing and high-throughput genotyping of 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 for Psm. PPR336 has been shown to stabilize mitochondrial ribosomes in Arabidopsis thaliana. Because MSC16 shows reduced transcription of rps7, a key component of mitochondrial ribosomes, PPR336 as the candidate for Psm is consistent with a nuclear effect on ribosome stability or assembly in the mitochondrion. We used polymorphisms in PPR336 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 MSC mitochondria is almost always lethal. This research demonstrates the usefulness of the MSC mutants of cucumber to study important mitochondrial-nuclear interactions and will be of interest to geneticists and breeders studying the plant organelles.

Technical Abstract: Cucumber (Cucumis sativus L.) is a useful plant to study organellar-nuclear interactions because its three genomes show differential transmission: bi-parental nuclear, maternal chloroplast and paternal mitochondrial (mt). The mt DNA of cucumber is relatively large due in part to accumulation of repetitive DNAs. Recombination among these repetitive regions produces structurally polymorphic mt DNAs associated with paternally transmitted, strongly mosaic (MSC) phenotypes. Mitochondrial mutant MSC16 possesses an under-representation of the rps7 gene, which encodes ribosomal protein S7 crucial for assembly 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. When a female plant is homozygous for Psm+ allele and is crossed with MSC16 as the male, almost all progeny show the MSC phenotype. When the female plant is homozygous for the Psm- allele, essentially all progenies produced from crosses with MSC16 as the male are wild-type. Using next-generation sequencing and high-throughput genotyping of 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 for Psm. PPR336 has been shown to stabilize mitochondrial ribosomes in Arabidopsis thaliana. Because MSC16 shows reduced transcription of rps7, a key component of mitochondrial ribosomes, PPR336 as the candidate for Psm is consistent with a nuclear effect on ribosome stability or assembly in the mitochondrion. We used polymorphisms in PPR336 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 MSC mitochondria is almost always lethal. This research demonstrates the usefulness of the MSC mutants of cucumber to study important mitochondrial-nuclear interactions.