Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica - PubMed (original) (raw)

Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica

Shengxin Chang et al. BMC Genomics. 2011.

Abstract

Background: Angiosperm mitochondrial genomes are more complex than those of other organisms. Analyses of the mitochondrial genome sequences of at least 11 angiosperm species have showed several common properties; these cannot easily explain, however, how the diverse mitotypes evolved within each genus or species. We analyzed the evolutionary relationships of Brassica mitotypes by sequencing.

Results: We sequenced the mitotypes of cam (Brassica rapa), ole (B. oleracea), jun (B. juncea), and car (B. carinata) and analyzed them together with two previously sequenced mitotypes of B. napus (pol and nap). The sizes of whole single circular genomes of cam, jun, ole, and car are 219,747 bp, 219,766 bp, 360,271 bp, and 232,241 bp, respectively. The mitochondrial genome of ole is largest as a resulting of the duplication of a 141.8 kb segment. The jun mitotype is the result of an inherited cam mitotype, and pol is also derived from the cam mitotype with evolutionary modifications. Genes with known functions are conserved in all mitotypes, but clear variation in open reading frames (ORFs) with unknown functions among the six mitotypes was observed. Sequence relationship analysis showed that there has been genome compaction and inheritance in the course of Brassica mitotype evolution.

Conclusions: We have sequenced four Brassica mitotypes, compared six Brassica mitotypes and suggested a mechanism for mitochondrial genome formation in Brassica, including evolutionary events such as inheritance, duplication, rearrangement, genome compaction, and mutation.

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Figures

Figure 1

Figure 1

Cytogenetic relationships of six cultivated Brassica species as depicted by U's triangle [20]. U's triangle illustrates the evolutionary relationship between three cultivated elementary species (B. rapa, B. oleracea, and B. nigra) and three amphiploid species (B. napus, B. juncea, and B. carinata). Chromosome numbers, nuclear genome types and mitotypes are shown inside or outside the circle for each species.

Figure 2

Figure 2

Large repeats exist in the six mitotypes. RB, R1, R, and R2 denote repeats of more than 2 kb. RB and R1 are shared by the six mitotypes, but their copy numbers vary.

Figure 3

Figure 3

Rearrangements of Brassica mitochondrial genomes. Syntenic regions > 2 kb are shown. (A) Rearrangement of the cam mitochondrial genome with the ole mitotype as a reference. (B) Rearrangement of the car mitochondrial genome with the ole mitotype as a reference. The numbers refer to the syntenic regions derived from a paired comparison. Highly or completely homologous regions are indicated by color.

Figure 4

Figure 4

Short repeats associated with changes in the mitochondrial genome of Brassica. The orientation of the sequence is shown by an arrow. (A) Repeat Q is possibly related to the influence of the rearrangement of syntenic regions 7, 2, 5, 6, 8, and 1 of the ole and cam mitotypes. (B) Repeat P may be related to the rearrangement of regions 16 and 1 in the ole and car mitotypes.

Figure 5

Figure 5

Clustering tree of Brassica mitotypes. It's according to the distance based on indels > 400 bp and SNPs (see Additional file 1, Tables S4 and S5).

Figure 6

Figure 6

Hypothesis regarding the evolution of six cultivated Brassica mitotypes. Diverse Brassica mitotypes are hypothesized to have evolved from an expanded ancestral parent mitotype and formed through mitochondrial genome speciation and compaction. Jun (B. juncea) is derived from the cam mitotype and pol and nap from a primary mitotype very similar to the cam mitotype, without deletion of the CMS-related orf224 gene region (4.4 kb) or its homolog orf222. The maternal mitotype from which car is derived is unclear (dotted lines). Three mitotypes for the elementary species are also hypothesized to be compaction forms from the large ancestral mitotype.

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