| Summary: | <p>Abstract</p> <p>Background</p> <p>The Streptophyta comprises all land plants and six groups of charophycean green algae. The scaly biflagellate <it>Mesostigma viride </it>(Mesostigmatales) and the sarcinoid <it>Chlorokybus atmophyticus </it>(Chlorokybales) represent the earliest diverging lineages of this phylum. In trees based on chloroplast genome data, these two charophycean green algae are nested in the same clade. To validate this relationship and gain insight into the ancestral state of the mitochondrial genome in the Charophyceae, we sequenced the mitochondrial DNA (mtDNA) of <it>Chlorokybus </it>and compared this genome sequence with those of three other charophycean green algae and the bryophytes <it>Marchantia polymorpha </it>and <it>Physcomitrella patens</it>.</p> <p>Results</p> <p>The <it>Chlorokybus </it>genome differs radically from its 42,424-bp <it>Mesostigma </it>counterpart in size, gene order, intron content and density of repeated elements. At 201,763-bp, it is the largest mtDNA yet reported for a green alga. The 70 conserved genes represent 41.4% of the genome sequence and include <it>nad10 </it>and <it>trnL</it>(gag), two genes reported for the first time in a streptophyte mtDNA. At the gene order level, the <it>Chlorokybus </it>genome shares with its <it>Chara</it>, <it>Chaetosphaeridium </it>and bryophyte homologues eight to ten gene clusters including about 20 genes. Notably, some of these clusters exhibit gene linkages not previously found outside the Streptophyta, suggesting that they originated early during streptophyte evolution. In addition to six group I and 14 group II introns, short repeated sequences accounting for 7.5% of the genome were identified. Mitochondrial trees were unable to resolve the correct position of <it>Mesostigma</it>, due to analytical problems arising from accelerated sequence evolution in this lineage.</p> <p>Conclusion</p> <p>The <it>Chlorokybus </it>and <it>Mesostigma </it>mtDNAs exemplify the marked fluidity of the mitochondrial genome in charophycean green algae. The notion that the mitochondrial genome was constrained to remain compact during charophycean evolution is no longer tenable. Our data raise the possibility that the emergence of land plants was not associated with a substantial gain of intergenic sequences by the mitochondrial genome.</p>
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