Max-Planck-Institut für Züchtungsforschung, Köln, Germany
Correspondence: E-mail: leister{at}mpiz-koeln.mpg.de.
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Abstract |
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Key Words: duplication gene transfer genome evolution mitochondria NUMT pseudogene
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Both the mitochondrial and the nuclear genome sequence are known for 13 eukaryotic species. Employing BLASTN searches at a range of different threshold levels allowed us to identify diverged and/or small NUMTs, as well as conserved and/or long ones. The result is that dramatic differences in the content of NUMTs in the different genomes are evident (fig. 1a): at a threshold of 104 they range from less than ten in Fugu, Drosophila, Plasmodium, and Caenorhabditis to more than 500 in human, rice, and Arabidopsis. Between 10 and 100 NUMTs are present in rat, Ciona, Neurospora, and in the yeast species. No NUMTs at all have been detected in Anopheles. For N. crassa only a preliminary estimate is possible because sequence information of its mtDNA is still incomplete; nevertheless, between 11 (threshold <1050) and 22 (104) NUMTs exist in this fungal species (fig. 1a).
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Then what is the reason behind the variable abundance of NUMTs in different species? Two explanations can be suggested. (1) The frequency of DNA transfer from mitochondria to the nucleus differs between species. The mtDNA escape into the cytoplasm, and ultimately its transfer to the nucleus, can be influenced by the vulnerability of mitochondria to stress and other factors (Bensasson et al. 2001a; Woischnik and Moraes 2002), as well as by the number of mitochondria present in each cellparticularly of the germline. Accordingly, species-specific differences in the formation of the germline and/or the number of mitochondria per cell may account for some of the interspecific differences in NUMT abundance observed. The number of mitochondria per cell could, for instance, explain the low number of NUMTs in Plasmodiuman organism having only one mitochondrion per cell (Divo et al. 1985; Hopkins et al. 1999). Furthermore, the number of somatic cell divisions from zygote to meiosis (and the loss of the nuclear envelope during each division) should influence the frequency of mitochondrion-to-nucleus DNA transfer (Walbot and Evans 2003). This might be the reason for the high NUMT content in the plants rice and Arabidopsis. Also, the efficiency of nuclear import of mtDNA and/or of its integration into the nuclear genome might differ between species. (2) The rate of loss of NUMTs is different among species. The rate and spectrum of DNA loss from the nucleus might shape the accumulation and size pattern of NUMTs. A specific spectrum of DNA loss could favor the deletion of NUMTs while still allowing the accumulation of massive amounts of noncoding DNA elements with different size. This type of DNA loss could lead to genomes with a large fraction of noncoding DNA but only with few NUMTs. Vice versa, a different control on DNA loss would allow more compact genomes to accumulate many NUMTs (such as in Arabidopsis). It is well known that the rate of DNA loss varies substantially for different fragment sizes and among species (Petrov et al. 2000; Bensasson et al. 2001b; Devos, Brown, and Bennetzen 2002), and this could explain the absence of a strict correlation between the abundances of noncoding nuclear DNA and NUMTs.
In conclusion, the causes for the interspecific diversity of NUMTs with respect to both copy number and length distribution remain obscure. The analysis of additional eukaryotic genomes to be completely sequenced in the future, in combination with the experimental analysis of the rates of mtDNA migration to the nucleusparticularly in related species that differ dramatically in their NUMT contentsshould shed light onto the question how and to which extent eukaryotes deal with NUMTs and other pseudogenes in their genomes.
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Materials and Methods |
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NCBI-BLASTN (Altschul et al. 1990) was carried out locally with standard settings and thresholds ranging from 104 to <1050. Whole mitochondrial genomes were BLASTed either against draft nuclear genome sequences (human, mouse, rice, and rat) or, in all other cases, against complete genomes.
Numbers for total genome sizes and the amount of intergenic sequences were extracted from the Web pages listed above. Values of nonprotein-coding DNA listed in table 1 were extracted from Taft and Mattick (2003).
Web Site
When additional genome sequences become available, updated versions of figure 1 and table 1 will be made available at: http://www.mpiz-koeln.mpg.de/leister/mbe_2004.html.
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Acknowledgements |
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Footnotes |
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Literature Cited |
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Allen, J. F. 1993. Control of gene expression by redox potential and the requirement for chloroplast and mitochondrial genomes. J. Theor. Biol. 165:609-631.[CrossRef][ISI][Medline]
Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.[CrossRef][ISI][Medline]
Bensasson, D., M. W. Feldman, and D. A. Petrov. 2003. Rates of DNA duplication and mitochondrial DNA insertion in the human genome. J. Mol. Evol. 57:343-354.[CrossRef][ISI][Medline]
Bensasson, D., D. A. Petrov, D. X. Zhang, D. L. Hartl, and G. M. Hewitt. 2001b. Genomic gigantism: DNA loss is slow in mountain grasshoppers. Mol. Biol. Evol. 18:246-253.
Bensasson, D., D. Zhang, D. L. Hartl, and G. M. Hewitt. 2001a. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol. Evol. 16:314-321.[CrossRef][ISI][Medline]
Bensasson, D., D. X. Zhang, and G. M. Hewitt. 2000. Frequent assimilation of mitochondrial DNA by grasshopper nuclear genomes. Mol. Biol. Evol. 17:406-415.
Devos, K. M., J. K. Brown, and J. L. Bennetzen. 2002. Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res. 12:1075-1079.
Divo, A. A., T. G. Geary, J. B. Jensen, and H. Ginsburg. 1985. The mitochondrion of Plasmodium falciparum visualized by rhodamine 123 fluorescence. J. Protozool. 32:442-446.[ISI][Medline]
Hartl, D. L. 2000. Molecular melodies in high and low C. Nat. Rev. Genet. 1:145-149.[CrossRef][ISI][Medline]
Hazkani-Covo, E., R. Sorek, and D. Graur. 2003. Evolutionary dynamics of large numts in the human genome: rarity of independent insertions and abundance of post-insertion duplications. J. Mol. Evol. 56:169-174.[CrossRef][ISI][Medline]
Henze, K., and W. Martin. 2001. How do mitochondrial genes get into the nucleus? Trends Genet. 17:383-387.[CrossRef][ISI][Medline]
Hopkins, J., R. Fowler, S. Krishna, I. Wilson, G. Mitchell, and L. Bannister. 1999. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150:283-295.[ISI][Medline]
Lopez, J. V., N. Yuhki, R. Masuda, W. Modi, and S. J. O'Brien. 1994. Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. J. Mol. Evol. 39:174-190.[ISI][Medline]
Mourier, T., A. J. Hansen, E. Willerslev, and P. Arctander. 2001. The Human Genome Project reveals a continuous transfer of large mitochondrial fragments to the nucleus. Mol. Biol. Evol. 18:1833-1837.
Petrov, D. A. 2001. Evolution of genome size: new approaches to an old problem. Trends Genet. 17:23-28.[CrossRef][ISI][Medline]
Petrov, D. A., T. A. Sangster, J. S. Johnston, D. L. Hartl, and K. L. Shaw. 2000. Evidence for DNA loss as a determinant of genome size. Science 287:1060-1062.
Ricchetti, M., C. Fairhead, and B. Dujon. 1999. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402:96-100.[CrossRef][ISI][Medline]
Sunnucks, P., and D. F. Hales. 1996. Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol. Biol. Evol. 13:510-524.[Abstract]
Taft, R. J., and J. S. Mattick. 2003. Increasing biological complexity is positively correlated with the relative genome-wide expansion of non-protein-coding DNA sequences. Genome Biology http://genomebiology.com/2003/5/I/PI.
Tourmen, Y., O. Baris, P. Dessen, C. Jacques, Y. Malthiery, and P. Reynier. 2002. Structure and chromosomal distribution of human mitochondrial pseudogenes. Genomics 80:71-77.[CrossRef][ISI][Medline]
Walbot, V., and M. M. Evans. 2003. Unique features of the plant life cycle and their consequences. Nat. Rev. Genet. 4:369-379.[CrossRef][ISI][Medline]
Woischnik, M., and C. T. Moraes. 2002. Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res. 12:885-893.
Zhang, D. X., and G. M. Hewitt. 1996. Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol. Evol. 11:247-251.[CrossRef][ISI]