Abstract
BackgroundPlant mitochondria, semiautonomous organelles that function as manufacturers of cellular ATP, have their own genome that has a slow rate of evolution and rapid rearrangement. Cytoplasmic male sterility (CMS), a common phenotype in higher plants, is closely associated with rearrangements in mitochondrial DNA (mtDNA), and is widely used to produce F1 hybrid seeds in a variety of valuable crop species. Novel chimeric genes deduced from mtDNA rearrangements causing CMS have been identified in several plants, such as rice, sunflower, pepper, and rapeseed, but there are very few reports about mtDNA rearrangements in wheat. In the present work, we describe the mitochondrial genome of a wheat K-type CMS line and compare it with its maintainer line.ResultsThe complete mtDNA sequence of a wheat K-type (with cytoplasm of Aegilops kotschyi) CMS line, Ks3, was assembled into a master circle (MC) molecule of 647,559 bp and found to harbor 34 known protein-coding genes, three rRNAs (18 S, 26 S, and 5 S rRNAs), and 16 different tRNAs. Compared to our previously published sequence of a K-type maintainer line, Km3, we detected Ks3-specific mtDNA (> 100 bp, 11.38%) and repeats (> 100 bp, 29 units) as well as genes that are unique to each line: rpl5 was missing in Ks3 and trnH was absent from Km3. We also defined 32 single nucleotide polymorphisms (SNPs) in 13 protein-coding, albeit functionally irrelevant, genes, and predicted 22 unique ORFs in Ks3, representing potential candidates for K-type CMS. All these sequence variations are candidates for involvement in CMS. A comparative analysis of the mtDNA of several angiosperms, including those from Ks3, Km3, rice, maize, Arabidopsis thaliana, and rapeseed, showed that non-coding sequences of higher plants had mostly divergent multiple reorganizations during the mtDNA evolution of higher plants.ConclusionThe complete mitochondrial genome of the wheat K-type CMS line Ks3 is very different from that of its maintainer line Km3, especially in non-coding sequences. Sequence rearrangement has produced novel chimeric ORFs, which may be candidate genes for CMS. Comparative analysis of several angiosperm mtDNAs indicated that non-coding sequences are the most frequently reorganized during mtDNA evolution in higher plants.
Highlights
Plant mitochondria, semiautonomous organelles that function as manufacturers of cellular ATP, have their own genome that has a slow rate of evolution and rapid rearrangement
We used similarity searches (BLAST and transfer RNA (tRNA) scan-SE) and found 53 genes in total; among them, we identified 34 known protein-coding genes, three ribosomal RNA (rRNA) (18 S, 26 S, and 5 S rRNAs), and 16 tRNAs, accounting for 6.22% of the genome (Additional File 1)
We revealed 38 segments of more than 100 bp in Ks3 mitochondrial DNA (mtDNA) that were not maintained in Km3 mtDNA (Figure 2 Additional Files 3 and 4) and totaled 73,670 bp (11.38%), ranging in size from 120 to 6371 bp and interspersed over 62 locations in the Ks3 master circle (MC) molecule
Summary
Semiautonomous organelles that function as manufacturers of cellular ATP, have their own genome that has a slow rate of evolution and rapid rearrangement. Cytoplasmic male sterility (CMS), a common phenotype in higher plants, is closely associated with rearrangements in mitochondrial DNA (mtDNA), and is widely used to produce F1 hybrid seeds in a variety of valuable crop species. CMS is a common phenotype in higher plants, and is closely associated with mutations in mtDNAs that cause pollen abortion. MtDNAs in higher plants are known to have the ability to undergo extensive recombination, resulting in sequence rearrangements. When these rearrangements produce “chimeric genes”, they may directly or indirectly alter normal physiological functions, such as pollen abortion. Comparative analysis of mtDNAs between a CMS line and its normal fertile counterpart should lead to the molecular details underlying the sterility phenotype in higher plants
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