Why Sequence Seed Plant Mitochondria?

Plant mitochondrial genomes are one of the last great frontiers for comparative sequencing. Our knowledge of these genomes comes from mapping studies, extensive Southern blot surveys, and very limited sequencing. Furthermore, compared to chloroplast genomes, they have been little used in reconstructing plant phylogeny. Plant mitochondrial genomes have been sequenced from only four angiosperms and one nonvascular plant. The goal of this project is to sequence 60 seed plant mitochondrial genomes of exceptional interest and promise for understanding both genome evolution and plant phylogeny.

Plant mitochondrial DNAs (mtDNAs) have long been known to possess many unusual, if not unique, properties. These include the lowest known rates of synonymous substitution (50-100 times lower than that in animal mitochondrial genomes) and exceptionally high rates of inversion and other internal rearrangements. (Two plant mtDNAs can have >99% sequence identity yet be highly scrambled in gene order!) Plant mtDNAs also have complex structural heterogeneity (i.e., a ‘master’ chromosome and subgenomic chromosomes resulting from high-frequency recombination between large direct repeats). Plant mitochondrial genomes are the largest of all known organelle genomes (200-2,400 Kb, 1-2 orders of magnitude larger than most mtDNAs, rivaling some bacterial genomes). Plant mtDNAs also frequently and persistently incorporate chloroplast and nuclear sequences, some of which are used in the mitochondria (e.g., captured chloroplast tRNA genes--no other organellar genomes take up exogenous cellular DNA like this).

Recent studies further underscore the dynamic and remarkable nature of plant mitochondrial genomes. For example, certain plant mtDNAs have been found to be extraordinarily active in functionally transferring their genes to the nucleus, whereas this process has virtually ceased among animals and fungi. Plant mtDNAs are also remarkably active in horizontal transfer of both mobile introns and standard genes; indeed, plant mtDNAs are the only genomes of multicellular eukaryotes found to transfer genes horizontally within a phylum. Finally, two plant groups have independently and recently experienced sudden, major (hundreds-fold), reversible changes in rates of mitochondrial (but not chloroplast or nuclear) synonymous substitution. So many fascinating properties of plant mtDNAs have now been revealed that comprehensive comparative genome sequencing is imperative. This work will provide a much deeper and richer understanding of several of these exciting phenomena (especially the functional transfer of mitochondrial genomes to the nucleus and the evolution of highly variable nucleotide substitution rates) and will help resolve a number of major unsolved issues in seed plant phylogeny.

CSP project participants: Jeffrey D. Palmer (proposer, Indiana Univ.), Jeffrey L. Boore (JGI and Univ. of California, Berkeley), and Eric B. Knox (Rutgers Univ. and Indiana Univ.).