Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants

Ayliffe, MA; Scott, N. Steele; Timmis, Jeremy N.

doi:10.1093/oxfordjournals.molbev.a025977

Cited by 66 publications

(50 citation statements)

References 31 publications

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“…The mismatch can be restored to the G-C pair in one direction, but creates an A-T pair in the other direction (Holliday and Grigg 1993;Finnegan et al 1998), resulting in T / C transitions (and A / G on the opposite strand). This observation is consistent with the known high level of C methylation in plant nuclear DNA (Ayliffe et al 1998) and with assuming no purifying selection on the sequence of ITS2 as may be expected if the ITS-B1-type genes do not contribute to the ribosome population. The origin of the G / T substitutions is not clear and G / A is not overrepresented.…”

Section: Resultssupporting

confidence: 90%

Molecular Evidence for Transcription of Genes on a B Chromosome in Crepis capillaris

et al. 2005

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Dispensable, supernumerary (B) chromosomes are found in diverse eukaryotic species. The origin and genetic consequences of B chromosomes have been the subjects of speculation for more than a century. Until now, there has been no molecular evidence that B chromosome DNA is transcribed and there is no unequivocal evidence as to their origin. B chromosomes are considered to be genetically inert although they appear to cause a variety of phenotypic effects. We report that members of one of two ribosomal RNA gene families that are confined to the B chromosomes of a plant, Crepis capillaris, are transcribed-thus providing the first molecular evidence of gene activity on B chromosomes. Sequence analysis of part of the A and B chromosome rRNA genes, together with comparisons with related species, indicates that the B chromosome rRNA genes originate from the A chromosome.

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Section: Resultssupporting

confidence: 90%

Molecular Evidence for Transcription of Genes on a B Chromosome in Crepis capillaris

et al. 2005

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“…Since organellar genomes are of bacterial origin, they exhibit mainly methylation of adenines and not of cytosines (Vanyushin and Ashapkin, 2011). Integration of organellar sequences in the nuclear genome is very common in many plant species, especially those that are outbreeding and have large genomes (Ayliffe et al, 1998). Seeing that over 99% of plastid and 95% of mitochondrial genomic sequences have at least one copy in the maize nuclear genome (Kumar and Bendich, 2011), we most likely are visualizing DNA methylation in the nuclear copies.…”

Section: Differential Methylation Targets 59 and 39 Edges Of Genic Rementioning

confidence: 99%

Differential Methylation during Maize Leaf Growth Targets Developmentally Regulated Genes

et al. 2014

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DNA methylation is an important and widespread epigenetic modification in plant genomes, mediated by DNA methyltransferases (DMTs). DNA methylation is known to play a role in genome protection, regulation of gene expression, and splicing and was previously associated with major developmental reprogramming in plants, such as vernalization and transition to flowering. Here, we show that DNA methylation also controls the growth processes of cell division and cell expansion within a growing organ. The maize (Zea mays) leaf offers a great tool to study growth processes, as the cells progressively move through the spatial gradient encompassing the division zone, transition zone, elongation zone, and mature zone. Opposite to de novo DMTs, the maintenance DMTs were transcriptionally regulated throughout the growth zone of the maize leaf, concomitant with differential CCGG methylation levels in the four zones. Surprisingly, the majority of differentially methylated sequences mapped on or close to gene bodies and not to repeat-rich loci. Moreover, especially the 59 and 39 regions of genes, which show overall low methylation levels, underwent differential methylation in a developmental context. Genes involved in processes such as chromatin remodeling, cell cycle progression, and growth regulation, were differentially methylated. The presence of differential methylation located upstream of the gene anticorrelated with transcript expression, while gene body differential methylation was unrelated to the expression level. These data indicate that DNA methylation is correlated with the decision to exit mitotic cell division and to enter cell expansion, which adds a new epigenetic level to the regulation of growth processes.DNA methylation is the covalent modification of nucleotides in DNA by the addition of a methyl group. In the nuclear genome of higher eukaryotes, 5-methylcytosine is the most important DNA modification (Goll and Bestor, 2005). It is a phenomenon of ancient origin predating plant-animal diversification. However, some differences exist between plant and animal methylome patterning and function, and DNA methylation has been found to be evolutionarily lost in a few species (Feng et al., 2010;Zemach et al., 2010). Eukaryotic DNA methylation is established by DNA methyltransferase (DMT) enzymes that transfer a methyl group from S-adenosyl Met to the fifth carbon of cytosine. These enzymes can largely be subdivided in maintenance and de novo DMTs, depending on whether the recognition site is already methylated or not. Maintenance DMTs conserve the methylation status of symmetrical (palindromic) sites after DNA replication, by recognizing the hemimethylated locus and methylating the newly synthesized strand. In plants, there are two types of maintenance DMTs: DNA METHYLTRANSFERASE (MET) and CHROMOMETHYLASE (CMT). The former methylates CG sites during DNA replication, whereas the latter methylates CHG (H = A, C, or T) sites located in chromatin in which histone 3 is dimethylated on Lys-9 (Goll and Bestor, 2005). De no...

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“…2B). HpaII restricts unmethylated plastid DNA, while methylated nuclear genome remains essentially intact (Ayliffe et al, 1998). If the PCR specifically amplifies nupts, there should be no reduction in the intensity of the amplified fragment when HpaII-digested DNA is used as template.…”

Section: Specific Amplification Of Nupt Sequences Inmentioning

confidence: 99%

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

2011

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The nuclear genome of eukaryotes contains large amounts of cytoplasmic organelle DNA (nuclear integrants of organelle DNA [norgs]). The recent sequencing of many mitochondrial and chloroplast genomes has enabled investigation of the potential role of norgs in endosymbiotic evolution. In this article, we describe a new polymerase chain reaction-based method that allows the identification and evolutionary study of recent and older norgs in a range of eukaryotes. We tested this method in the genus Nicotiana and obtained sequences from seven nuclear integrants of plastid DNA (nupts) totaling 25 kb in length. These nupts were estimated to have been transferred 0.033 to 5.81 million years ago. The spectrum of mutations present in the potential protein-coding sequences compared with the noncoding sequences of each nupt revealed that nupts evolve in a nuclear-specific manner and are under neutral evolution. Indels were more frequent in noncoding regions than in potential coding sequences of former chloroplastic DNA, most probably due to the presence of a higher number of homopolymeric sequences. Unexpectedly, some potential protein-coding sequences within the nupts still contained intact open reading frames for up to 5.81 million years. These results suggest that chloroplast genes transferred to the nucleus have in some cases several millions of years to acquire nuclear regulatory elements and become functional. The different factors influencing this time frame and the potential role of nupts in endosymbiotic gene transfer are discussed.More than a billion years ago, the ancestors of mitochondria and plastids were free-living eubacteria that were sequentially engulfed by a precursor of the nucleated cell (Timmis et al., 2004). Since these two separate endosymbiotic events, organelle DNA has been continuously transferred and integrated into the nucleus. Insertions of organelle DNA are referred to as numts (nuclear integrants of mitochondrial DNA; Lopez et al., 1994) and nupts (nuclear integrants of plastid DNA; Timmis et al., 2004) or collectively as norgs (nuclear integrants of organelle DNA; Leister, 2005). Transfer of mitochondrial and plastid DNA to the nucleus has been shown to occur at a very high frequency ( Thorsness and Fox, 1990;Huang et al., 2003;Stegemann et al., 2003;Sheppard et al., 2008). Several molecular mechanisms involved in the integration of mitochondrial DNA into the nucleus have been suggested and are likely to be similar for nupts.These include the degradation and lysis of mitochondria, the encapsulation of mitochondrial DNA inside the nucleus, the direct physical association between the mitochondria and nucleus with membrane fusions, or the entry and incorporation of mitochondrial DNA into nuclear chromosomes (for review, see Hazkani-Covo et al., 2010). During evolution, this DNA transfer and integration into the nucleus have resulted in the functional relocation of many organelle genes in the nucleus, leading to a massive reduction in the size of organelle genomes compared with those of their fr...

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Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants

Cited by 66 publications

References 31 publications

Molecular Evidence for Transcription of Genes on a B Chromosome in Crepis capillaris

Molecular Evidence for Transcription of Genes on a B Chromosome in Crepis capillaris

Differential Methylation during Maize Leaf Growth Targets Developmentally Regulated Genes

Conservation of Plastid Sequences in the Plant Nuclear Genome for Millions of Years Facilitates Endosymbiotic Evolution

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