Accelerated evolution of the mitochondrial genome in an alloplasmic line of durum wheat

Abstract

BackgroundWheat is an excellent plant species for nuclear mitochondrial interaction studies due to availability of large collection of alloplasmic lines. These lines exhibit different vegetative and physiological properties than their parents. To investigate the level of sequence changes introduced into the mitochondrial genome under the alloplasmic condition, three mitochondrial genomes of the Triticum-Aegilops species were sequenced: 1) durum alloplasmic line with the Ae. longissima cytoplasm that carries the T. turgidum nucleus designated as (lo) durum, 2) the cytoplasmic donor line, and 3) the nuclear donor line.ResultsThe mitochondrial genome of the T. turgidum was 451,678 bp in length with high structural and nucleotide identity to the previously characterized T. aestivum genome. The assembled mitochondrial genome of the (lo) durum and the Ae. longissima were 431,959 bp and 399,005 bp in size, respectively. The high sequence coverage for all three genomes allowed analysis of heteroplasmy within each genome. The mitochondrial genome structure in the alloplasmic line was genetically distant from both maternal and paternal genomes. The alloplasmic durum and the Ae. longissima carry the same versions of atp6, nad6, rps19-p, cob and cox2 exon 2 which are different from the T. turgidum parent. Evidence of paternal leakage was also observed by analyzing nad9 and orf359 among all three lines. Nucleotide search identified a number of open reading frames, of which 27 were specific to the (lo) durum line.ConclusionsSeveral heteroplasmic regions were observed within genes and intergenic regions of the mitochondrial genomes of all three lines. The number of rearrangements and nucleotide changes in the mitochondrial genome of the alloplasmic line that have occurred in less than half a century was significant considering the high sequence conservation between the T. turgidum and the T. aestivum that diverged from each other 10,000 years ago. We showed that the changes in genes were not limited to paternal leakage but were sufficiently significant to suggest that other mechanisms, such as recombination and mutation, were responsible. The newly formed ORFs, differences in gene sequences and copy numbers, heteroplasmy, and substoichiometric changes show the potential of the alloplasmic condition to accelerate evolution towards forming new mitochondrial genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-67) contains supplementary material, which is available to authorized users.

The role of mitochondria in plant development and stress tolerance

“…Molecular analyses are only beginning to address the functional implications of the alloplasmic condition. For instance, comparative analysis of the mitochondrial genomes among a wheat alloplasmic line and its two parents indicated accelerated evolution of the mtDNA under the alloplasmic condition resulting in SNP variation and structural rearrangements (NOYSZEWSKI et al 2014). Detailed analysis of one particular mitochondrial gene essential to ATP production, ATP synthase subunit 6 (ATP6), revealed moderate SNP variation, but much more substantial structural and presence/absence variation across the Triticum-Aegilops complex, suggesting rearrangements as the predominate evolutionary driving force in the mitochondria (SOLTANI et al 2014).…”

Mitochondrial genome and transcriptome analysis of five alloplasmic male-sterile lines in Brassica juncea

“…CMS often develops when the cytoplasm, donated by wild relative, is incompatible with cultivar-derived nucleus, and the specific Rf gene is located within the genome of the wild relative. These types of alloplasmic lines often retain mitochondrial segments derived from the wild donor, also defined as mitotype-specific sequences (MSSs) [50], and is most often observed in wheat [51, 52] and Brassicas [53–55].…”

Analysis ofATP6sequence diversity in theTriticum–Aegilopsspecies group reveals the crucial role of rearrangement in mitochondrial genome evolution

“…1). In silico translation revealed that ATP6-1a encodes a 386 amino acid (aa) polypeptide with a high degree of similarity to the ATP6-1 protein present in T. aestivum (Ogihara et al 2005) and T. turgidum mitochondrion (Noyszewski et al 2014). The ATP6-1b encodes a 415 aa protein, which is identical to a previously reported gene in Ae.…”