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An unexpectedly large and loosely packed mitochondrial genome in the charophycean green alga Chlorokybus atmophyticus (Turmel et al., 2007)

This article shows that mitochondrial genomes can be quite different between organisms, especially in early branching organisms. I am not too familiar with plants, but this reported genome look more eukaryotic-like than bacterial-like. At the moment just for reference, don’t know what to make from it, short of a good predictive model for the acquisition of the genome.

 

Abstract: The Streptophyta comprises all land plants and six groups of charophycean green algae. The scaly biflagellate Mesostigma viride (Mesostigmatales) and the sarcinoid Chlorokybus atmophyticus (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 Chlorokybus and compared this genome sequence with those of three other charophycean green algae and the bryophytes Marchantia polymorpha and Physcomitrella patens. The Chlorokybus genome differs radically from its 42,424-bp Mesostigma 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 nad10 and trnL(gag), two genes reported for the first time in a streptophyte mtDNA. At the gene order level, the Chlorokybus genome shares with its Chara, Chaetosphaeridium 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 Mesostigma, due to analytical problems arising from accelerated sequence evolution in this lineage. The Chlorokybus and Mesostigma 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.

From the intro: We report here that the Chlorokybus mitochondrial genome differs dramatically from Mesostigma mtDNA at the levels of size, gene order and intron content. Although the Chlorokybus genome is substantially larger than any other green algal mtDNA characterized yet, its gene organization features a pronounced degree of ancestral features. Our findings provide new light into mitochondrial genome evolution in the Streptophyta.

Highly variable gene density in charophycean mitochondrial genomes

Larger than other Charophyceans, Chlorokybus is most loosely packed mitochondrial genome so far, challenged concept that constraints in evolution were to minimize genome size, prominent size & low gene density

Contrasting evolutionary trends of the mitochondrial genome in the Chlorokybus
and Mesostigma lineages:

Chlorokybus is closely related to Mesostigma [13]. In light of this close relationship, our finding that the Chlorokybus mitochondrial genome differs considerably from its Mesostigma counterpart not only in gene density but also in gene order came as a surprise. No specifically shared genomic features could be identified in these charophycean mitochondrial genomes.

The Chlorokybus mitochondrial genome has retained numerous ancestral characters at the gene content and gene organizational levels. This genome is the most gene-rich among the green algal mtDNAs sequenced thus far and features two genes that have not been reported to be mtDNA-encoded in streptophytes prior to our study [nad10 and trnL(gag)], thus bringing to 75 the number of genes making up the gene repertoire of the common ancestor of all streptophytes (Table 2). Of these genes, seven (rpl2, rps1, sdh3, sdh4, yejR, yejU and yejV) are not found in the Chlorophyta. The mitochondrial genome sequences currently available for chlorophytes suggest that the gene repertoire of the common ancestor of these algae was more limited and included 70 genes, only two of which are not present in the Streptophyta [rnpB and trnT(ugu)].

Like its bryophyte counterparts, the Chlorokybus mitochondrial genome has maintained several ancestral gene clusters even though short repeated sequences and spacious intergenic regions increase opportunities for gene rearrangements [44, 51]. On the other hand, clear evidence that rearrangements affected a few ancestral clusters comes from the observation that the Chlorokybus genome has not preserved the eubacteria-like arrangement of the ribosomal protein genes corresponding to the contiguous S10, spc and α operons of Escherichia coli (the cluster corresponding to the 11-gene segment delimited by rps10 and rps11 in Marchantia) as well as the nad5-nad4-nad2 cluster, both of which are found in the Chaetosphaeridium, Chara and the two bryophyte genomes. Interestingly, some of the eight to ten clusters shared by Chlorokybus and other streptophyte mtDNAs (Table 3) exhibit gene linkages [rps2-trnF(gga), trnP(ugg)-sdh3 and nd4L-trnY(gua)] that have not been documented outside the Streptophyta, suggesting that they arose very early during streptophyte evolution

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