Nuclear insertions of organellar DNA can create novel patches of functional exon sequences

Noutsos, Christos; Kleine, Tatjana; Armbruster, Ute; DalCorso, Giovanni; Leister, Dario

doi:10.1016/j.tig.2007.08.016

Cited by 70 publications

(81 citation statements)

References 25 publications

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“…These transplastomic assays have shown that plastomic DNA is transferred to the nucleus in very large, sometimes scrambled (17), sections, and bioinformatic evidence shows that the process also involves small pieces of the DNA (8,9,11,17). However, there is no experimental evidence of small de novo inserts of plastid DNA analogous to the mitochondrial sequences that we demonstrated by DSB induction and smPCR.…”

Section: Discussionmentioning

confidence: 78%

“…Although these transplastomics are initially able to show only DNA movement per se, subsequent rearrangements within the nucleus have been shown to activate prokaryotic genes in ways that recapitulate real endosymbiotic evolution (16,17). The profound global consequences of the processes that are made possible by initial DNA transfer are fully revealed by bioinformatic analyses showing how endosymbiotic evolution has contributed thousands of genes to the eukaryotic nucleus (9,10,(33)(34)(35). This deluge of cytoplasmic organellar DNA into the nucleus (31) clearly results in a "trialand-error" system of genomic rearrangements after which a few integrants gain functionality.…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

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confidence: 99%

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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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Section: Discussionmentioning

confidence: 78%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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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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“…Although most such transfers involve small, apparently random fragments of organellar DNA that have no notable impact on the nuclear genome, entire genes can be transferred and expressed in their new environment (for example, see refs 39, 40). Instances in which NUMTs have altered existing genes by introducing new introns or truncating the gene through frameshifts have also been observed (for example, see refs [41][42][43].…”

Section: Why Do Nucleomorphs Persist?mentioning

confidence: 99%

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

Curtis

Tanifuji

Burki

et al. 2012

Nature

357

398

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“…Although DNA transfer is frequent, functional gene transfer of organelle genes is very rare since expression requires the acquisition of nuclear gene regulatory elements and, usually, a target peptide if the protein is to replace the organellar equivalent (Stegemann and Bock, 2006;Lloyd and Timmis, 2011). In addition, insertions of organelle DNA have created new genes and nuclear exons encoding parts of novel proteins (Noutsos et al, 2007;Kleine et al, 2009) and novel putative nuclear gene regulatory elements (Knoop and Brennicke, 1991). Analysis of the Arabidopsis (Arabidopsis thaliana), rice (Oryza sativa), Chlamydomonas reinhardtii, and Cyanidioschyzon merolae proteomes suggest that about 14% of nuclear genes are of plastid origin (Deusch et al, 2008).…”

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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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Nuclear insertions of organellar DNA can create novel patches of functional exon sequences

Cited by 70 publications

References 25 publications

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

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

Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs

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

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