Ins and outs of plant mitochondrial genome evolution.

Abstract

Although intracellular DNA transfer is regarded as quite a general phenomenon in flowering plants, little is known about the extent of interorganellar DNA transfer or the mechanism(s) involved in the transfer processes. DNA transfer into, and out of, a range of flowering plant mitochondrial genomes has been examined. Transfer of chloroplast DNA (cpDNA) sequences into the mitochondrion was investigated in six species of plants within the crucifer family. Only a small fraction (2-6%) of the mitochondrial genome in crucifers is chloroplast-derived; phylogenetic evidence suggests that a serial transfer of cpDNA into the mitochondrial genome has occurred over evolutionary time. Despite their apparent non-functionality in crucifer mitochondrial DNAs (mtDNAs), transferred cpDNA sequences are maintained within mitochondrial genomes over long periods of time. MtDNAs from 20 flowering plant species were screened with probes specific for all of the available flowering plant mitochondrial protein genes and their introns. The results of this survey suggest that mitochondrial gene content and intron content have remained quite constant during the evolution of flowering plants. Three gene linkages are conserved in all 20 mitochondrial genomes examined. Only four genes (coxII, rps13, rps14, and atp8) and three introns (coxII intron and nad4 introns 2 and 3) failed to hybridize to all of the mtDNAs examined. Loss of the mitochondrial coxII gene is tolerated in legumes because a copy of coxII was transferred to and became functional in the nucleus during flowering plant evolution. The nuclear coxII gene more closely resembles edited mitochondrial coxII transcripts than the genes encoding these mRNAs. Hence gene transfer appears to have involved reverse transcription of an edited RNA intermediate. A comparison between the Brassica campestris mitochondrial gene map and the B. campestris mitochondrial transcript map suggests that flowering plant mtDNAs may contain significantly more genes than previously estimated. The B. campestris mitochondrial nad6 gene has been characterized. This is the first nad6 gene isolated from a flowering plant mitochondrial genome. Southern blot hybridization indicates that nad6 is present in the mtDNA of all of a wide range of flowering plant species examined.