ANRV375-PP60-06 ARI 25 March 2009 13:13 DNA Transfer from Organelles to the Nucleus: The Idiosyncratic Genetics of Endosymbiosis Tatjana Kleine,1 Uwe G. Maier,2 and Dario Leister1 1Lehrstuhl fur¨ Botanik, Department Biologie I; Ludwig-Maximilians-Universitat¨ Munchen,¨ 82152 Planegg-Martinsried, Germany; email: [email protected]; [email protected] 2Cell Biology, Philipps-Universitat¨ Marburg, 35032 Marburg, Germany; email: [email protected] Annu. Rev. Plant Biol. 2009. 60:115–38 Key Words First published online as a Review in Advance on gene evolution, gene transfer, genome evolution, plastid, November 17, 2008 mitochondrion, NUMTs, NUPTs The Annual Review of Plant Biology is online at plant.annualreviews.org Abstract This article’s doi: In eukaryotes, DNA is exchanged between endosymbiosis-derived com- 10.1146/annurev.arplant.043008.092119 partments (mitochondria and chloroplasts) and the nucleus. Organelle- Copyright c 2009 by Annual Reviews. to-nucleus DNA transfer involves repair of double-stranded breaks by All rights reserved nonhomologous end-joining, and resulted during early organelle evo- 1543-5008/09/0602-0115$20.00 lution in massive relocation of organelle genes to the nucleus. A large Annu. Rev. Plant Biol. 2009.60:115-138. Downloaded from www.annualreviews.org fraction of the products of the nuclear genes so acquired are retargeted Access provided by University of British Columbia on 12/21/17. For personal use only. to their ancestral compartment; many others now function in new sub- cellular locations. Almost all present-day nuclear transfers of mitochon- drial or plastid DNA give rise to noncoding sequences, dubbed nuclear mitochondrial DNAs (NUMTs) and nuclear plastid DNAs (NUPTs). Some of these sequences were recruited as exons, thus introducing new coding sequences into preexisting nuclear genes by a novel mechanism. In organisms derived from secondary or tertiary endosymbiosis, serial gene transfers involving nucleus-to-nucleus migration of DNA have also occurred. Intercompartmental DNA transfer therefore represents a significant driving force for gene and genome evolution, relocating and refashioning genes and contributing to genetic diversity. 115 ANRV375-PP60-06 ARI 25 March 2009 13:13 in plants, at least five have been observed Contents (Figure 1). Transfer of DNA from mitochondrion or INTRODUCTION .................. 116 plastid to the nucleus has significantly shaped GENETIC AND GENOMIC eukaryotic genomes; during the early phase of CONSEQUENCES OF organelle evolution, transfer of DNA from or- INTERCOMPARTMENTAL ganelle to nucleus resulted in a massive reloca- DNA TRANSFER ................ 117 tion of organelle genes. Conversely, the appar- Transfer of Entire Genes ent absence of sequences of nuclear origin in to the Nucleus .................. 117 plastid DNAs (ptDNAs) implies that nucleus- Other Types of Intercompartmental to-plastid transfer occurs extremely rarely, if Gene Transfer .................. 121 at all, whereas evidence for mitochondrion- DNA Transfer Resulting in to-plastid gene transfer in a green alga was Acquisition of Noncoding provided recently. Among the promiscuous Nuclear Sequences: NUMTs DNA sequences originating from nucleus-to- and NUPTs .................... 122 mitochondrion and plastid-to-mitochondrion Generation of Novel Nuclear Exons 125 transfer only plastid-derived mitochondrial Nuclear DNA Transfer in Organisms tRNA genes are functional (see section be- Derived from Secondary low entitled Transfer of Entire Genes to the and Tertiary Endosymbiosis ..... 125 Nucleus). MECHANISMS...................... 127 Although the movement of certain mito- The Nature of the Migrant chondrial and plastid genes to the nucleus Nucleic Acid.................... 127 has occurred quite frequently in flowering Escape of DNA from Organelles.... 128 plants during evolutionarily recent times (1), Mechanisms of DNA Integration in many eukaryotes (including animals) the at the Molecular Level .......... 129 transfer of functional genes is now rare or EVOLUTIONARY has ceased altogether (17). Nevertheless, DNA CONSEQUENCES ............... 130 transfer from organelle to nucleus is an ongo- CONCLUDING REMARKS ......... 131 ing and ubiquitous process. Almost all present- day nuclear transfers of mitochondrial DNA (mtDNA) and ptDNA give rise to noncod- INTRODUCTION ing sequences, dubbed nuclear mitochondrial In eukaryotes, DNA molecules are found in DNAs (NUMTs) (72) and nuclear plastid several distinct cellular compartments: the nu- DNAs (NUPTs) (134). Analysis of such se- cleus, mitochondria, and, in the case of algae quences has allowed the reconstruction of many Annu. Rev. Plant Biol. 2009.60:115-138. Downloaded from www.annualreviews.org and plants, plastids. Mitochondria and plastids aspects of the mechanisms of DNA integra- Access provided by University of British Columbia on 12/21/17. For personal use only. descended respectively from α-proteobacteria- tion into the nucleus and thrown much light like and cyanobacteria-like prokaryotes by en- on the evolutionary forces acting on noncod- dosymbiosis, but they contain much less DNA ing DNA sequences (see section below enti- than their contemporary prokaryotic relatives. tled DNA Transfer Resulting in Acquisition of This loss of DNA is caused, over evolution- Noncoding Nuclear Sequences: NUMTs and ary time, by the redistribution of genetic ma- NUPTs).More recently, researchers discovered terial between nucleus, mitochondria and plas- an intermediate between the transfer of en- tids via intercompartmental DNA transfer—a tire genes and the generation of noncoding se- NUMTs: nuclear mitochondrial DNAs phenomenon discovered more than 25 years quences: NUMTsand NUPTscan be recruited ago (34, 127, 135, 141). Of the six types of as novel exons for preexisting nuclear genes NUPTs: nuclear plastid DNAs DNA transfer that are theoretically possible (see section below entitled Generation of Novel among the three genetic compartments present Nuclear Exons). 116 Kleine · Maier · Leister ANRV375-PP60-06 ARI 25 March 2009 13:13 In algae derived from secondary or ter- Plastid tiary endosymbiosis, complex plastids with ad- ditional genetic compartments were initially Mitochondrion present. This presence adds an extra level of 5 complexity to intercompartmental DNA trans- fer and permits serial DNA transfers, involv- 3 ing the remobilization of previously transferred DNA DNA (see section below entitled Nuclear DNA Transferin Organisms Derived from Secondary DNA and Tertiary Endosymbiosis). The systematic analyses of insertions of organelle DNA in the 1 4 2 nuclear genomes of humans, Arabidopsis, and rice, as well as experiments designed to trace nuclear gene transfer under laboratory condi- tions, have provided insights into the mode of origin and divergence of nuclear organelle DNA (see section below entitled Mechanisms). The role of nuclear DNA transfer in gene and genome evolution was obviously crucial in the era of large-scale gene transfer from organelles to the nucleus, whereas the evolutionary im- pact of NUMTsand NUPTsis less well defined (see section below entitled Evolutionary Con- Nucleus sequences). In this review, we summarize recent Figure 1 progress in the field of organelle-to-nucleus Overview of known types of interorganelle DNA transfer: (1) mitochondrion- transfer of DNA, with particular reference to to-nucleus, (2) plastid-to-nucleus, (3) plastid-to-mitochondrion, (4) nucleus- to-mitochondrion, and (5) mitochondrion-to-plastid. The thickness of the lines the transfers associated with the cyanobacte- indicates the frequency of events detected in contemporary plant genomes. rial endosymbiosis that led to the evolution of the green lineage of photoautotrophs, and we emphasize the underlying cellular and ge- their genomes now encode only a small fraction netic mechanisms and their evolutionary con- of the organelle’s proteins, ranging from 3 sequences. to 67 in mitochondria and from 15 to 209 in plastids (reviewed in Reference 58). This reduction is the consequence of the loss or GENETIC AND GENOMIC transfer of endosymbiotic genes to the nucleus Secondary (tertiary) Annu. Rev. Plant Biol. 2009.60:115-138. Downloaded from www.annualreviews.org CONSEQUENCES OF of the host, a special form of horizontal (or endosymbiosis: Access provided by University of British Columbia on 12/21/17. For personal use only. INTERCOMPARTMENTAL lateral) gene transfer that is associated with engulfment and DNA TRANSFER the gradual loss of the organelle’s genetic retention by another autonomy (66, 68, 78, 134). On the basis of free-living eukaryote Transfer of Entire Genes of a product of the composition of the gene sets that remain to the Nucleus primary (secondary) in plastids and mitochondria, most organelle endosymbiosis Both mitochondria and plastids are of genes are thought to have been transferred in Complex plastids: endosymbiotic origin: They are descen- early (and perhaps rapid) migrations, whereas plastids that derive dants of α-proteobacterium-like (4) and subsequent transfers are thought to have been from secondary or cyanobacterium-like (104) [more specifically, highly discontinuous (reviewed in Reference tertiary endosymbiosis; heterocyst-forming (31)] progenitors, respec- 58). A nuclear copy of an organelle gene must typically surrounded by more than two tively. Although the organelles have retained acquire additional genetic elements if it is to membranes much of their prokaryotic biochemistry (134), remain functional in its new environment.