Palindromic sequences and A+T-rich DNA elements promote illegitimate recombination in Nicotiana tabacum

Müller, Andreas E.; Kamisugi, Yasuko; Grüneberg, R; Niedenhof, Ingrid; Hörold, R.J; Meyer, Peter

doi:10.1006/jmbi.1999.2957

Cited by 63 publications

(34 citation statements)

References 80 publications

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“…All transplastomic DNA sequences adjacent to junction sites terminated at different, apparently random, positions of the transplastome with no insertional preference for AT-or T-rich sequences as previously observed in biolistic-and͞or Agrobacterium-mediated DNA integration (22)(23)(24)(25)(26).…”

Section: New Nupts Are Generally Larger Than the Transcripts Of Selecsupporting

confidence: 58%

“…These include nonhomologous recombination between transferred ptDNA fragments (kr1, kr5, and kr10); scrambling of transplastomic DNA sequences in the nuclear genomic DNA (kr17-2); incorporation of filler DNA between disjunct regions of ptDNA (kr5-1), from neighboring ptDNA (kr18-2), or from an unknown source (kr5-2); formation of complex nuclear loci with multiple ptDNA integrants ( Table 2); and the presence of microhomology (2-5 bp) near the transplastomic junctions (J1b, J5-1b, J7a, and J10a). The junction sequences display many of the hallmarks of nonhomologous recombination, and their organization is reminiscent of nuclear integrants after biolistic and T-DNA delivery (27,(29)(30)(31)(32), although they show no sequence preference for the ATand T-rich sequences observed in both biolistic and T-DNA transformation (22)(23)(24)(25)(26). We have not been able to obtain a complete picture of any native integration sites before nupt insertion, although several nuclear junctions were obtained.…”

Section: New Nupts Are Generally Larger Than the Transcripts Of Selecmentioning

confidence: 90%

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Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco

Huang

Ayliffe

Timmis

2004

Proc. Natl. Acad. Sci. U.S.A.

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Transfer of organelle DNA into the nuclear genome has been significant in eukaryotic evolution, because it appears to be the origin of many nuclear genes. Most studies on organelle DNA transfer have been restricted to evolutionary events but experimental systems recently became available to monitor the process in real time. We designed an experimental screen to detect plastid DNA (ptDNA) transfers to the nucleus in whole plants grown under natural conditions. The resultant genotypes facilitated investigation of the evolutionary mechanisms underlying ptDNA transfer and nuclear integration. Here we report the characterization of nuclear loci formed by integration of newly transferred ptDNA. Large, often multiple, fragments of ptDNA between 6.0 and 22.3 kb in size are incorporated into chromosomes at single Mendelian loci. The lack of chloroplast transcripts of comparable size to the ptDNA integrants suggests that DNA molecules are directly involved in the transfer process. Microhomology (2-5 bp) and rearrangements of ptDNA and nuclear DNA were frequently found near integration sites, suggesting that nonhomologous recombination plays a major role in integration. The mechanisms of ptDNA integration appear similar to those of biolistic transformation of plant cells, but no sequence preference was identified near junctions. This article provides substantial molecular analysis of real-time ptDNA transfer and integration that has resulted from natural processes with no involvement of cell injury, infection, and tissue culture. We highlight the impact of cytoplasmic organellar genome mobility on nuclear genome evolution.

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Section: New Nupts Are Generally Larger Than the Transcripts Of Selecsupporting

confidence: 58%

Section: New Nupts Are Generally Larger Than the Transcripts Of Selecmentioning

confidence: 90%

Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco

Huang

Ayliffe

Timmis

2004

Proc. Natl. Acad. Sci. U.S.A.

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“…Illegitimate recombination can occur by different mechanisms (reviewed by Mü ller et al, 1999). In the 'breakage-and-rejoining' model, free DNA ends can be joined either by direct ligation of blunt ends or by pairing of single-stranded cohesive ends mediated by short stretches (2-6 bp) of homology (microhomologies).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary dynamics and sites of illegitimate recombination revealed in the interspersion and sequence junctions of two nonhomologous satellite DNAs in cactophilic Drosophila species

et al. 2009

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Satellite DNA (satDNA) is a major component of genomes but relatively little is known about the fine-scale organization of unrelated satDNAs residing at the same chromosome location, and the sequence structure and dynamics of satDNA junctions. We studied the organization and sequence junctions of two nonhomologous satDNAs, pBuM and DBC-150, in three species from the neotropical Drosophila buzzatii cluster (repleta group). In situ hybridization to microchromosomes, interphase nuclei and extended DNA fibers showed frequent interspersion of the two satellites in D. gouveai, D. antonietae and, to a lesser extent, D. seriema. We isolated by PCR six pBuM Â DBC-150 junctions: four are exclusive to D. gouveai and two are exclusive to D. antonietae. The six junction breakpoints occur at different positions within monomers, suggesting independent origin. Four junctions showed abrupt transitions between the two satellites, whereas two junctions showed a distinct 10 bp tandem duplication before the junction. Unlike pBuM, DBC-150 junction repeats are more variable than randomly cloned monomers and showed diagnostic features in common to a 3-monomer higher-order repeat seen in the sister species D. serido. The high levels of interspersion between pBuM and DBC-150 repeats suggest extensive rearrangements between the two satellites, maybe favored by specific features of the microchromosomes. Our interpretation is that the junctions evolved by multiples events of illegitimate recombination between nonhomologous satDNA repeats, with subsequent rounds of unequal crossing-over expanding the copy number of some of the junctions.

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“…This likely leads to the accumulation of mutagenic factors as observed here, including microsatellites, long homopolymer stretches, forward or palindromic repeats of any length, and a low GC content (Table 1, Figure 2; see Supplemental Figures 2 and 3 online). Those elements increase intramolecular and illegitimate recombination (Ogihara et al, 1988;Fejes et al, 1990;Sears et al, 1996;Müller et al, 1999;Gray et al, 2009;Maréchal and Brisson, 2010), which in turn may cause the deletion of dispensable plastome fragments. Graphical summary of the number of gene losses (A) and the losses of functional classes of genes (B) based on the reconstruction of plastid gene contents at ancestral nodes in Orobanchaceae.…”

Section: Evolution Of Chromosomal Size and Architecture After The Losmentioning

confidence: 99%

Mechanisms of Functional and Physical Genome Reduction in Photosynthetic and Nonphotosynthetic Parasitic Plants of the Broomrape Family

Müller²,

et al. 2013

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(G.M.S.).Nonphotosynthetic plants possess strongly reconfigured plastomes attributable to convergent losses of photosynthesis and housekeeping genes, making them excellent systems for studying genome evolution under relaxed selective pressures. We report the complete plastomes of 10 photosynthetic and nonphotosynthetic parasites plus their nonparasitic sister from the broomrape family (Orobanchaceae). By reconstructing the history of gene losses and genome reconfigurations, we find that the establishment of obligate parasitism triggers the relaxation of selective constraints. Partly because of independent losses of one inverted repeat region, Orobanchaceae plastomes vary 3.5-fold in size, with 45 kb in American squawroot (Conopholis americana) representing the smallest plastome reported from land plants. Of the 42 to 74 retained unique genes, only 16 protein genes, 15 tRNAs, and four rRNAs are commonly found. Several holoparasites retain ATP synthase genes with intact open reading frames, suggesting a prolonged function in these plants. The loss of photosynthesis alters the chromosomal architecture in that recombinogenic factors accumulate, fostering large-scale chromosomal rearrangements as functional reduction proceeds. The retention of DNA fragments is strongly influenced by both their proximity to genes under selection and the cooccurrence with those in operons, indicating complex constraints beyond gene function that determine the evolutionary survival time of plastid regions in nonphotosynthetic plants.

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Palindromic sequences and A+T-rich DNA elements promote illegitimate recombination in Nicotiana tabacum

Cited by 63 publications

References 80 publications

Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco

Simple and complex nuclear loci created by newly transferred chloroplast DNA in tobacco

Evolutionary dynamics and sites of illegitimate recombination revealed in the interspersion and sequence junctions of two nonhomologous satellite DNAs in cactophilic Drosophila species

Mechanisms of Functional and Physical Genome Reduction in Photosynthetic and Nonphotosynthetic Parasitic Plants of the Broomrape Family

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