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Intergenomic gene transfer in diploid and allopolyploid Gossypium.

ABSTRACT: BACKGROUND:Intergenomic gene transfer (IGT) between nuclear and organellar genomes is a common phenomenon during plant evolution. Gossypium is a useful model to evaluate the genomic consequences of IGT for both diploid and polyploid species. Here, we explore IGT among nuclear, mitochondrial, and plastid genomes of four cotton species, including two allopolyploids and their model diploid progenitors (genome donors, G. arboreum: A2 and G. raimondii: D5). RESULTS:Extensive IGT events exist for both diploid and allotetraploid cotton (Gossypium) species, with the nuclear genome being the predominant recipient of transferred DNA followed by the mitochondrial genome. The nuclear genome has integrated 100 times more foreign sequences than the mitochondrial genome has in total length. In the nucleus, the integrated length of chloroplast DNA (cpDNA) was between 1.87 times (in diploids) to nearly four times (in allopolyploids) greater than that of mitochondrial DNA (mtDNA). In the mitochondrion, the length of nuclear DNA (nuDNA) was typically three times than that of cpDNA. Gossypium mitochondrial genomes integrated three nuclear retrotransposons and eight chloroplast tRNA genes, and incorporated chloroplast DNA prior to divergence between the diploids and allopolyploid formation. For mitochondrial chloroplast-tRNA genes, there were 2-6 bp conserved microhomologies flanking their insertion sites across distantly related genera, which increased to 10 bp microhomologies for the four cotton species studied. For organellar DNA sequences, there are source hotspots, e.g., the atp6-trnW intergenic region in the mitochondrion and the inverted repeat region in the chloroplast. Organellar DNAs in the nucleus were rarely expressed, and at low levels. Surprisingly, there was asymmetry in the survivorship of ancestral insertions following allopolyploidy, with most numts (nuclear mitochondrial insertions) decaying or being lost whereas most nupts (nuclear plastidial insertions) were retained. CONCLUSIONS:This study characterized and compared intracellular transfer among nuclear and organellar genomes within two cultivated allopolyploids and their ancestral diploid cotton species. A striking asymmetry in the fate of IGTs in allopolyploid cotton was discovered, with numts being preferentially lost relative to nupts. Our results connect intergenomic gene transfer with allotetraploidy and provide new insight into intracellular genome evolution.

SUBMITTER: Zhao N

PROVIDER: S-EPMC6852956 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsRepetitive DNA sequences are thought to be involved in the formation of chromosomal rearrangements. The aim of this study was to analyse the distribution of microsatellite clusters in Aegilops biuncialis and Aegilops geniculata, and its relationship with the intergenomic translocations in these allotetraploid species, wild genetic resources for wheat improvement.MethodsThe chromosomal localization of (ACG)(n) and (GAA)(n) microsatellite sequences in Ae. biuncialis and Ae. geniculata and in their diploid progenitors Aegilops comosa and Aegilops umbellulata was investigated by sequential in situ hybridization with simple sequence repeat (SSR) probes and repeated DNA probes (pSc119·2, Afa family and pTa71) and by dual-colour genomic in situ hybridization (GISH). Thirty-two Ae. biuncialis and 19 Ae. geniculata accessions were screened by GISH for intergenomic translocations, which were further characterized by fluorescence in situ hybridization and GISH.Key resultsSingle pericentromeric (ACG)(n) signals were localized on most U and on some M genome chromosomes, whereas strong pericentromeric and several intercalary and telomeric (GAA)(n) sites were observed on the Aegilops chromosomes. Three Ae. biuncialis accessions carried 7U(b)-7M(b) reciprocal translocations and one had a 7U(b)-1M(b) rearrangement, while two Ae. geniculata accessions carried 7U(g)-1M(g) or 5U(g)-5M(g) translocations. Conspicuous (ACG)(n) and/or (GAA)(n) clusters were located near the translocation breakpoints in eight of the ten translocated chromosomes analysed, SSR bands and breakpoints being statistically located at the same chromosomal site in six of them.ConclusionsIntergenomic translocation breakpoints are frequently mapped to SSR-rich chromosomal regions in the allopolyploid species examined, suggesting that microsatellite repeated DNA sequences might facilitate the formation of those chromosomal rearrangements. The (ACG)(n) and (GAA)(n) SSR motifs serve as additional chromosome markers for the karyotypic analysis of UM genome Aegilops species.

Project description:BackgroundCotton (Gossypium spp.) is commonly grouped into eight diploid genomic groups and an allotetraploid genomic group, AD. The mitochondrial genomes supply new information to understand both the evolution process and the mechanism of cytoplasmic male sterility. Based on previously released mitochondrial genomes of G. hirsutum (AD1), G. barbadense (AD2), G. raimondii (D5) and G. arboreum (A2), together with data of six other mitochondrial genomes, to elucidate the evolution and diversity of mitochondrial genomes within Gossypium.ResultsSix Gossypium mitochondrial genomes, including three diploid species from D and three allotetraploid species from AD genome groups (G. thurberi D1, G. davidsonii D3-d and G. trilobum D8; G. tomentosum AD3, G. mustelinum AD4 and G. darwinii AD5), were assembled as the single circular molecules of lengths about 644 kb in diploid species and 677 kb in allotetraploid species, respectively. The genomic structures of mitochondrial in D group species were identical but differed from the mitogenome of G. arboreum (A2), as well as from the mitogenomes of five species of the AD group. There mainly existed four or six large repeats in the mitogenomes of the A + AD or D group species, respectively. These variations in repeat sequences caused the major inversions and translocations within the mitochondrial genome. The mitochondrial genome complexity in Gossypium presented eight unique segments in D group species, three specific fragments in A + AD group species and a large segment (more than 11 kb) in diploid species. These insertions or deletions were most probably generated from crossovers between repetitive or homologous regions. Unlike the highly variable genome structure, evolutionary distance of mitochondrial genes was 1/6th the frequency of that in chloroplast genes of Gossypium. RNA editing events were conserved in cotton mitochondrial genes. We confirmed two near full length of the integration of the mitochondrial genome into chromosome 1 of G. raimondii and chromosome A03 of G. hirsutum, respectively, with insertion time less than 1.03 MYA.ConclusionTen Gossypium mitochondrial sequences highlight the insights to the evolution of cotton mitogenomes.

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Intergenomic gene transfer in diploid and allopolyploid Gossypium.

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