Extending the limited transfer window hypothesis to inter-organelle DNA migration

Abstract

Mitochondrial genomes often contain large amounts of plastid DNA (ptDNA)-derived sequences (MTPTs). It has been suggested that the intercompartmental transfer of ptDNA is greatly reduced in species with only a single plastid per cell (monoplastidic) as compared with those with many plastids per cell (polyplastidic). This hypothesis has not been applied to the movement of DNA from plastids to mitochondria. By analyzing the organelle genomes from diverse mono- and polyplastidic taxa, I show that MTPTs are restricted to the mitochondrial genomes of species with many plastids per cell and are absent from those with one plastid per cell or with monoplastidic meristematic systems. Moreover, the most bloated mitochondrial genomes that were explored had the largest MTPT contents. These data, like previous results on ptDNA-derived sequences in nuclear genomes, support the hypothesis that plastid number and the forces governing the expansion and contraction of noncoding mitochondrial DNA (mtDNA) influence MTPT abundance. I also show that plastid genomes are depauperate in mtDNA-derived sequences (PTMTs), irrespective of the number of mitochondria per cell and plastid genome size, which may reflect the lack of a DNA uptake system in plastids.

FIG. 1.—

Bar graph showing the number and accumulative length of ptDNA-derived sequences (MTPTs) within the mitochondrial genomes of various plastid-harboring eukaryotes. For references and notes on the number of organelles per cell, see table 1 and supplementary table S2 (Supplementary Material online).

FIG. 2.—

Plot of MTPT content versus mitochondrial genome size (log scale) (A) and mitochondrial genome noncoding DNA content (B). Species of particular interest are labeled on the plot. Data on mitochondrial genome size and noncoding DNA content are shown in supplementary table S1 (Supplementary Material online).