Fewer genes than organelles: extremely low and variable gene copy numbers in mitochondria of somatic plant cells

Abstract

SUMMARYPlant mitochondrial genomes are split into sub-genomes, i.e. genes are distributed across various sub-genomic molecules. To investigate whether copy numbers vary between individual mitochondrial genes, we used quantitative real-time PCR in combination with flow cytometric determination of nuclear DNA quantities to determine absolute per-cell-copy numbers of four mitochondrial genes in various Arabidopsis organs and the leaves of tobacco (Nicotiana tabacum) and barley (Hordeum vulgare). The copy numbers of the investigated mitochondrial genes (atp1, rps4, nad6 and cox1) not only differed from each other, but also varied between organs and changed during the development of cotyledons and leaves in Arabidopsis. We found no correlation between altered gene copy numbers, transcript levels and O 2 consumption. However, per cell, both the number of mitochondria and the number of gene copies increased with growing cell size. Gene copy numbers varied from approximately 40 (cox1 in young leaves) to approximately 280 (atp1 in mature leaves), and the mean number of mitochondria was approximately 300 in young leaves and 450 in mature leaves. Thus, cells are polyploid with respect to their mitochondrial genomes, but individual mitochondria may contain only part of the genome or even no DNA at all. Our data supports structural models of the mitochondrial genome in non-dividing cells of angiosperms that predict localization of the genes on sub-genomic molecules rather than master chromosomes. The data indicate control of the number of individual genes according to the genotype and developmental program(s) via amplification and/or degradation of sub-genomic molecules.

Divergent Roles for the Two PolI-Like Organelle DNA Polymerases of Arabidopsis

“…However, since wild-type and mutant plants of the same age are being compared, any variations in nuclear or organellar DNA levels should not affect our results. It is interesting that previous studies reported a similar trend for ptDNA (Zoschke et al, 2007) and mtDNA (Preuten et al, 2010) ratios in aging cotyledons of Arabidopsis, although different samples were used in these studies (cotyledon alone versus whole seedling with roots).…”

How do plants make mitochondria?

“…In Arabidopsis, the number of mitochondria per cell was found to increase with cell size and over development (Preuten et al 2010). Young leaves were observed to contain approximately 300 mitochondria per cell while older mature leaves were observed to have 450 mitochondria per cell (Preuten et al 2010). Variations in mitochondrial morphology and dynamics are also evident, with the movement, fusion and Wssion of mitochondria documented (Logan 2010).…”

“…In contrast, complex II abundance was found to be the inverse, as it was high in roots and callus tissue and lower in abundance in leaves and stems (Peters et al 2012). In Arabidopsis, the number of mitochondria per cell was found to increase with cell size and over development (Preuten et al 2010). Young leaves were observed to contain approximately 300 mitochondria per cell while older mature leaves were observed to have 450 mitochondria per cell (Preuten et al 2010).…”

Mitochondrial Energy and Redox Signaling in Plants

“…As a complication, mitochondrial DNA (mtDNA) is distributed highly heterogeneously across the individual discrete mitochondria of a plant cell that undergo frequent fusion and fission. Often, mitochondria only contain a substoichiometric amount of the full genome, and some mitochondria contain no mtDNA at all (6,170). For these mitochondria, CoRR requires additional features: upon a signal, fusion with a DNAcontaining mitochondrion needs to occur, so a change in gene expression can be achieved; alternatively, CoRR could act post-transcriptionally on mtRNA, which may be stored in mitochondria that do not contain any mtDNA.…”