Gene transfer from organelles to the nucleus: Frequent and in big chunks

Martin, William

doi:10.1073/pnas.1633606100

Cited by 190 publications

(148 citation statements)

References 34 publications

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“…This confirms previous findings that genes frequently are transferred from the chloroplast or mitochondrial genome to the nucleus, where they acquire new expression control and targeting signals for the correct expression, translation, and reimport into the organelle (Martin, 2003).…”

Section: Gene Content In Chloroplast and Mitochondrial Genomessupporting

confidence: 91%

Exploring the Plant Transcriptome through Phylogenetic Profiling

Vandepoele

Peer

2005

Plant Physiology

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Publicly available protein sequences represent only a small fraction of the full catalog of genes encoded by the genomes of different plants, such as green algae, mosses, gymnosperms, and angiosperms. By contrast, an enormous amount of expressed sequence tags (ESTs) exists for a wide variety of plant species, representing a substantial part of all transcribed plant genes. Integrating protein and EST sequences in comparative and evolutionary analyses is not straightforward because of the heterogeneous nature of both types of sequence data. By combining information from publicly available EST and protein sequences for 32 different plant species, we identified more than 250,000 plant proteins organized in more than 12,000 gene families. Approximately 60% of the proteins are absent from current sequence databases but provide important new information about plant gene families. Analysis of the distribution of gene families over different plant species through phylogenetic profiling reveals interesting insights into plant gene evolution, and identifies species-and lineage-specific gene families, orphan genes, and conserved core genes across the green plant lineage. We counted a similar number of approximately 9,500 gene families in monocotyledonous and eudicotyledonous plants and found strong evidence for the existence of at least 33,700 genes in rice (Oryza sativa). Interestingly, the larger number of genes in rice compared to Arabidopsis (Arabidopsis thaliana) can partially be explained by a larger amount of species-specific single-copy genes and species-specific gene families. In addition, a majority of large gene families, typically containing more than 50 genes, are bigger in rice than Arabidopsis, whereas the opposite seems true for small gene families.

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Section: Gene Content In Chloroplast and Mitochondrial Genomessupporting

confidence: 91%

Exploring the Plant Transcriptome through Phylogenetic Profiling

Vandepoele

Peer

2005

Plant Physiology

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“…Endosymbiotic gene transfer (EGT) from anciently acquired bacterial-derived organelles, namely the mitochondria (derived from a proteobacterium) and chloroplast (derived from a cyanobacterium), make up the majority of horizontally transferred genes found in eukaryotic genomes (42,65,66). DNA transfer from plastid and mitochondrial genomes to the nucleus, which include noncoding nuclear plastid DNA's (NUPTs) and nuclear mitochondrial DNAs (NUMTs), occurred at the time of endosymbiont acquisition and later in evolutionary time and likely occurs quite frequently in present time (65,(67)(68)(69)(70)(71). This is particularly true for photosynthetic organisms, where the majority of genes required for plastid function are actually housed in the nuclear genome, with a greatly reduced plastid genome from the original acquired state (72,73).…”

Section: Discussionmentioning

confidence: 99%

Diatom centromeres suggest a mechanism for nuclear DNA acquisition

Diner

Noddings

Lian

et al. 2017

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

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Centromeres are essential for cell division and growth in all eukaryotes, and knowledge of their sequence and structure guides the development of artificial chromosomes for functional cellular biology studies. Centromeric proteins are conserved among eukaryotes; however, centromeric DNA sequences are highly variable. We combined forward and reverse genetic approaches with chromatin immunoprecipitation to identify centromeres of the model diatom Phaeodactylum tricornutum. We observed 25 unique centromere sequences typically occurring once per chromosome, a finding that helps to resolve nuclear genome organization and indicates monocentric regional centromeres. Diatom centromere sequences contain low-GC content regions but lack repeats or other conserved sequence features. Native and foreign sequences with similar GC content to P. tricornutum centromeres can maintain episomes and recruit the diatom centromeric histone protein CENH3, suggesting nonnative sequences can also function as diatom centromeres. Thus, simple sequence requirements may enable DNA from foreign sources to persist in the nucleus as extrachromosomal episomes, revealing a potential mechanism for organellar and foreign DNA acquisition.diatom | Phaeodactylum tricornutum | episome | centromere | CENH3

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“…The experimental demonstration of DNA transfer from the chloroplast to the nucleus (3,4) showed such a high frequency as to make its implications controversial (31,32). Therefore, it is even more surprising to find that the rate of transfer is increased up to 10-fold by mild temperature stresses applied over short periods.…”

Section: Discussionmentioning

confidence: 99%

“…The ingress of cytoplasmic organellar DNA in tobacco grown in ideal environments is already considered remarkably high (31), and it must be mutagenic at rates equivalent to or exceeding any other causes (43). Clearly, eukaryotes evolved in the real world of highly variable growth conditions, and they must have been subject to massive oscillations in the rate of bombardment with cytoplasmic organellar DNA.…”

Section: Discussionmentioning

confidence: 99%

Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants

Wang

Lloyd

Timmis

2012

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

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Mitochondria and chloroplasts (photosynthetic members of the plastid family of cytoplasmic organelles) in eukaryotic cells originated more than a billion years ago when an ancestor of the nucleated cell engulfed two different prokaryotes in separate sequential events. Extant cytoplasmic organellar genomes contain very few genes compared with their candidate free-living ancestors, as most have functionally relocated to the nucleus. The first step in functional relocation involves the integration of inactive DNA fragments into nuclear chromosomes, and this process continues at high frequency with attendant genetic, genomic, and evolutionary consequences. Using two different transplastomic tobacco lines, we show that DNA migration from chloroplasts to the nucleus is markedly increased by mild heat stress. In addition, we show that insertion of mitochondrial DNA fragments during the repair of induced double-strand breaks is increased by heat stress. The experiments demonstrate that the nuclear influx of organellar DNA is a potentially a source of mutation for nuclear genomes that is highly susceptible to temperature fluctuations that are well within the range experienced naturally.D NA in the highly energetic cytoplasmic organellar genetic compartments of eukaryotes is subjected to high levels of stress damage from the oxygen free radicals produced during respiration and photosynthesis. Nonetheless, for various reasons, the rate of accumulation of mutations is slower in plant cytoplasmic organelles than in the nucleus (1, 2). The vast majority of mitochondrial and plastid (chloroplast) genes have vacated their ancestral prokaryote genetic compartment in favor of the nucleus (2), with very few remaining within extant organelles. The first step in gene relocation for the organelle genomes is DNA escape, followed by insertion into nuclear chromosomes, a process shown to occur remarkably frequently under normal physiological conditions in tobacco (3, 4) and yeast (5), although an experimental screen in the unicellular alga Chlamydomonas reinhardtii did not detect any such transpositions (6). These experimental studies, together with bioinformatic and genomic analyses (7)(8)(9)(10)(11)(12)(13)(14), demonstrated that DNA transfer from cytoplasmic organelles is a frequent and continuous process in essentially all eukaryotes examined, although it may be very rare in organisms with very low organelle numbers (15). Although DNA transfer per se is very frequent in higher plants, genes that migrate are normally inactive in the nucleus because they lack the motifs required for nuclear expression. Nonetheless, on rare occasions nuclear integrants of organelle DNA (norgs) are activated by genomic rearrangements (16,17), that effectively duplicate the gene. Over evolutionary time, these frequent nonfunctional and rare functional DNA transfer processes have resulted in the net loss of redundant genes in the cytoplasmic organelles and have added to the genetic complexity of the nucleus.Environmental factors are known to modify mitoch...

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Gene transfer from organelles to the nucleus: Frequent and in big chunks

Cited by 190 publications

References 34 publications

Exploring the Plant Transcriptome through Phylogenetic Profiling

Exploring the Plant Transcriptome through Phylogenetic Profiling

Diatom centromeres suggest a mechanism for nuclear DNA acquisition

Environmental stress increases the entry of cytoplasmic organellar DNA into the nucleus in plants

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