Plastidic trnF_UUC Pseudogenes in North American Genus Boechera (Brassicaceae): Mechanistic Aspects of Evolution

Abstract

The origin and maintenance of a plastidic tandem repeat next to the trnF_UUC gene were analyzed in the genus Boechera in a phylogenetic context and were compared to published analogous examples that emerged in parallel in the Asteraceae and Juncaceae, respectively. Although we identified some features common to these taxonomic groups with respect to structure and origin of the region, obvious differences were encountered, which argue against a specific mechanism or evolutionary principle underlying the parallel origin and maintenance of the trnF-tandem repeats in those families. In contrast to the situation in the Asteraceae, no reciprocal recombinant repeat types have been observed in the Brassicaceae. Forty copy types, classified into three groups, were isolated from 103 chloroplast haplotypes of Boechera and it was demonstrated that they are composed of four subregions of various origins. We discuss various mutation mechanisms such as DNA replication slippage, and inter- and intrachromosomal recombination which were reported to mediate variation in copy numbers and other types of observed sequence length polymorphism. It is shown that the observed molecular structure of the tandem repeat region did not fully fit the particular patterns expected under a scenario of evolution including any of the known mechanisms. Nevertheless, it appeared that intermolecular unequal crossing-over is most likely the driving force in the evolution of this tandem repeat. However, it remains to be explained, why no reciprocal recombinant copy types have been observed. The reconstructed phylogenetic relationships among copies reflected different evolutionary scenarios as follows: (1) A single and ancient origin of copies pre-dates the radiation of Boechera. (2) Parallel expansion and shortening of the tandem repeat within different Boechera lineages. (3) Conservation of the first copy, as it was the only one present in all chloroplast haplotypes.

Boechera - Brassicaceae - chloroplast DNA - evolution - molecular recombination - phylogeny - pseudogene - transposable elements

References

• 1 Avise J. C.. Molecular Markers, Natural History and Evolution. 2nd ed. Sunderland, MA; Sinauer (2004): 1-684
• 2 Bailey C. D., Price R. A., Doyle J. J.. Systematics of the halimolobine Brassicaceae: evidence from three loci and morphology.  Systematic Botany. (2002);  27 318-332
• 3 Bellstedt D. U., Linder H. P., Harley E. H.. Phylogenetic relationships in Disa based on non-coding trnL-trnF chloroplast sequences: evidence of numerous repeat regions.  American Journal of Botany. (2001);  88 2088-2100
• 4 Bi X., Liu L. F.. RecA-independent DNA recombination between repetitive sequences: mechanisms and implications.  Progress in Nucleic Acid Research and Molecular Biology. (1996);  54 253-292
• 5 Bingham S. E., Webber A. N.. Maintenance and expression of heterologous genes in chloroplast of Chlamydomonas reinhardtii.  Journal of Applied Phycology. (1994);  6 239-245
• 6 Birky C. M.. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models.  Annual Review of Genetics. (2001);  35 125-148
• 7 Blasko K., Kaplan S. A., Higgins K. G., Wolfson R., Sears B. B.. Variation in copy number of a 24-base pair tandem repeat in the chloroplast DNA of Oenothera hookeri strain Johansen.  Current Genetics. (1988);  14 287-292
• 8 Bleeker W., Hurka H.. Introgressive hybridization in Rorippa (Brassicaceae): gene flow and its consequences in natural and anthropogenic habitats.  Molecular Ecology. (2001);  10 2013-2022
• 9 Bonnard G., Weil J.-H., Steinmetz A.. The intergenic region between the Vicia faba chloroplast tRNA‐Leu (CAA) and tRNA-Leu (UAA) genes contains a partial copy of the split tRNA-Leu (UAA) gene.  Current Genetics. (1985);  9 417-422
• 10 Bornet B., Branchard M.. Non-anchored Inter Simple Sequence Repeat (ISSR) markers: reproducible and specific tools for genome fingerprinting.  Plant Molecular Biology Reporter. (2001);  19 209-215
• 11 Borsch T., Hilu K. W., Quandt D., Wilde V., Neinhuis C., Barthlott W.. Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms.  Journal of Evolutionary Biology. (2003);  16 558-576
• 12 Bzymek M., Lovettdagger S. T.. Instability of repetitive DNA sequences: the role of replication in multiple mechanisms.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 8319-8325
• 13 Casacuberta E., Casacuberta J. M., Puigodomènech P., Monfort A.. Presence of miniature inverted-repeat transposable elements (MITEs) in the genome of Arabidopsis thaliana: characterisation of the Emigrant family elements.  The Plant Journal. (1998);  16 79-85
• 14 Chiu W.-L., Sears B. B.. Recombination between chloroplast DNAs does not occur in sexual crosses of Oenothera.  Molecular and General Genetics. (1985);  198 525-528
• 15 Clegg M. T., Gaut B. S., Learn G. H., Morton B. R.. Rates and patterns of chloroplast DNA evolution.  Proceedings of the National Academy of Sciences of the USA. (1994);  91 6795-6801
• 16 Clauss M. J., Koch M.. Arabidopsis and its poorly known relatives.  Trends in Plant Science. (2006);  11 449-459
• 17 Cosner M. E., Jansen R. K., Palmer J. D., Downie, St. R.. The highly rearranged chloroplast genome of Trachelium caeruleum (Campanulaceae): multiple inversions, inverted repeat expansion and contraction, transposition, insertions/deletions, and several repeat families.  Current Genetics. (1997);  31 419-429
• 18 Cozzolino S., Cafasso D., Pellegrino G., Musacchio A., Widmer A.. Molecular evolution of a plastid tandem repeat locus in an orchid lineage.  Journal of Molecular Evolution. (2003);  57 S41-S49
• 19 Dally A. M., Second G.. Chloroplast DNA diversity in wild and cultivated species of rice (genus Oryza, section Oryza). Cladistic-mutation and genetic-distance analysis.  Theoretical and Applied Genetics. (1990);  80 209-222
• 20 Dauvillee D., Hilbig L., Preiss S., Johanningmeier U.. Minimal extent of sequence homology required for homologous recombination at the psbA locus in Chlamydomonas reinhardtii chloroplasts using PCR-generated DNA fragments.  Photosynthesis Research. (2004);  79 219-224
• 21 Dix P. J., Kavanagh T. A.. Transforming the plastome: genetic markers and DNA delivery systems.  Euphytica. (1995);  85 29-34
• 22 Dobeš C., Mitchell-Olds T., Koch M.. Extensive chloroplast haplotype variation indicates Pleistocene hybridization and radiation of North American Arabis drummondii, A. × divaricarpa, and A. holboellii (Brassicaceae).  Molecular Ecology. (2004);  13 349-370
• 23 Downie, St. R., Olmstead R. G., Zurawski G., Soltis D. E., Soltis P. S., Watson J. C., Palmer J. D.. Six independent losses of the chloroplast DNA rpl2 intron in dicotyledons: molecular and phylogenetic implications.  Evolution. (1991);  45 1245-1259
• 24 Drábková L., Kirschner J., Vlcek C., Paces V.. TrnL-trnF intergenic spacer and trnL intron define major clades within Luzula and Juncus (Juncaceae): importance of structural mutations.  Journal of Molecular Evolution. (2004);  59 1-10
• 25 Eichler E. E., Sankoff D.. Structural dynamics of eukaryotic chromosome evolution.  Science. (2003);  301 793-797
• 26 Eisen J. A.. Mechanistic basis of microsatellite instability. Goldstein, D. B. and Schlötterer, C., eds. Microsatellites. Evolution and Applications. New York; Oxford University Press (1999): 34-48
• 27 Erickson J. M., Rahire M., Rochaix J.-D., Mets L. J.. Herbicide resistance and cross-resistance: changes at three distinct sites in the herbicide-binding protein.  Science. (1986);  228 204-207
• 28 Fan W. H., Woelfle M. A., Mosig G.. Two copies of a DNA element, “Wendy”, in the chloroplast chromosome of Chlamydomonas reinhardtii between rearranged gene clusters.  Plant Molecular Biology. (1995);  29 63-80
• 29 Fedoroff N.. Transposons and genome evolution in plants.  Proceedings of the National Academy of Sciences of the USA. (2000);  97 7002-7007
• 30 Fejes E., Engler D., Maliga P.. Extensive homologous chloroplast recombination in pl 14 Nicotiana somatic hybrid.  Theoretical and Applied Genetics. (1990);  79 28-32
• 31 Feschotte C., Mouchès C.. Evidence that a family of miniature inverted-repeat transposable elements (MITEs) from Arabidopsis thaliana genome has arisen from a pogo-like DNA transposon.  Molecular Biology and Evolution. (2000);  17 730-737
• 32 Feuillet C., Keller B.. Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution.  Annals of Botany (London). (2002);  89 3-10
• 33 Galun E.. Transposable Elements. A Guide to the Perplexed and the Novice. Dordrecht, The Netherlands; Kluwer Academic Publishers (2003): 1-335
• 34 Glickman B. W., Ripley L. S.. Structural intermediates of deletion mutagenesis: a role for palindromic DNA.  Proceedings of the National Academy of Sciences of the USA. (1984);  81 512-516
• 35 Gopaul D. N., Van Duyne G. D.. Structure and mechansim in site-specific recombination.  Current Opinion in Structural Biology. (1999);  9 14-20
• 36 Govindaraju D. R., Dancik B. P., Wagner D. B.. Novel chloroplast DNA polymorphism in a sympatric region of two pines.  Journal of Evolutionary Biology. (1989);  2 49-59
• 37 Graham S. W., Reeves P. A., Burns A. C. E., Olmstead R. G.. Microstructural changes in non-coding chloroplast DNA: interpretation, evolution, and utility of indels and inversions in basal angiosperm phylogenetic inference.  International Journal of Plant Science. (2000);  161 S83-S96
• 38 Hallet B., Sherratt D. J.. Transposition and site-specific recombination: adapting DNA cut-and-paste mechanisms to a variety of genetic rearrangements.  FEMS Microbiology Reviews. (1997);  21 157-178
• 39 Heenan P. B., Mitchell A. D., Koch M.. Molecular systematics of the New Zealand Pachycladon (Brassicaceae) complex: generic circumscription and relationships to Arabidopsis s.l. and Arabis s.l.  New Zealand Journal of Botany. (2002);  40 543-562
• 40 Hilu K. W., Alice L. A.. Evolutionary implications of matK indels in Poaceae.  American Journal of Botany. (2005);  86 1735-1741
• 41 Hipkins V. D., Marshall K. A., Neale D. B., Rottmann W. H., Strauss S. H.. A mutation hotspot in the chloroplast genome of a conifer (Douglas-fir: Pseudotsuga) is caused by variability in the number of direct repeats derived from a partially duplicated tRNA gene.  Current Genetics. (1995);  27 572-579
• 42 Isoda K., Shiraishi S., Kisanuki H.. Classifying Abies species (Pinaceae) based on the sequence variation of a tandemly repeated array found in the chloroplast DNA trnL and trnF intergenic spacer.  Silvae Genetica. (2000);  49 161-165
• 43 Jaeger J. A., Turner D. H., Zuker M.. Improved predictions of secondary structures for RNA.  Proceedings of the National Academy of Sciences of the USA. (1989);  86 7706-7710
• 44 Kamiya K., Harada K., Clyde M. M., Mohamed A. L.. Genetic variation of Trigonobalanus verticillata, a primitive species of Fagaceae, in Malaysia revealed by chloroplast sequences and AFLP markers.  Genes and Genetic Systems. (2002);  77 177-186
• 45 Kanno A., Hirai A.. Comparative studies of the structure of chloroplast DNA from four species of Oryza: cloning and physical maps.  Theoretical and Applied Genetics. (2004);  83 791-798
• 46 Kanno A., Lee Y.-O., Kameya T.. The structure of chloroplast genome in members of the genus Asparagus.  Theoretical and Applied Genetics. (1997);  95 1196-1202
• 47 Kanno A., Watanabe N., Nakamura I., Hirai A.. Variations in chloroplast DNA from rice (Oryza sativa): differences between deletions mediated by short direct-repeats sequences within single species.  Theoretical and Applied Genetics. (1993);  86 579-584
• 48 Kato S., Yamaguchi H., Shimamoto Y., Mikami T.. The chloroplast genomes of azuki bean and its close relatives: a deletion mutation found in weed azuki bean.  Hereditas. (2000);  132 43-48
• 49 Kazazian Jr. H. H.. Mobile elements: drivers of genome evolution.  Science. (2004);  303 1626-1632
• 50 Kelchner S. A.. The evolution of non-coding chloroplast DNA and its application in plant systematics.  Annals of Missouri Botanical Garden. (2000);  87 482-498
• 51 Kelchner S. A., Clark L. G.. Molecular evolution and phylogenetic utility of the chloroplast rpl16 intron in Chusquea and the Bambusoideae (Poaceae).  Molecular Phylogenetics and Evolution. (1997);  8 385-397
• 52 King G. J.. Through a genome, darkly: comparative analysis of plant chromosomal DNA.  Plant Molecular Biology. (2002);  48 5-20
• 53 Kirti P. B., Mohapatra T., Baldev A., Prakash S., Chopra V. L.. A stable cytoplasmic male-sterile line of Brassica juncea carrying restructured organelle genomes from the somatic hybrid Trachystoma ballii + B. juncea.  Plant Breeding. (1995);  114 434-438
• 54 Kirti P. B., Narasimhulu S. B., Mohapatra T., Prakash S., Chopra V. L.. Correction of chlorophyll deficiency in alloplasmic male sterile Brassica juncea through recombination between chloroplast genomes.  Genetical Research. (1993);  62 11-14
• 55 Kluge A., Farris J.. Quanitative phyletics and the evolution of anurans.  Systematic Zoology. (1969);  18 1-32
• 56 Koch M., Dobeš C., Kiefer C., Schmickl R., Klimeš L., Lysak M. A.. Supernetwork identifies multiple events of plastid trnF_(GAA) pseudogene evolution in the Brassicaceae.  Molecular Biology and Evolution. (2007);  24 63-73
• 57 Koch M., Dobeš C., Matschinger M.. The trnF (GAA) gene in cruciferous plants: extensive duplication, variation in copy number and parallel evolution. 16th International Symposium Biodiversity and Evolutionary Biology of the German Botanical Society (DBG), 21. - 27. September, Frankfurt am Main. Palmarum Hortus Francofurtensis 7, 54. (2003 a)
• 58 Koch M., Dobeš C., Matschinger M., Ansell St., Bleeker W., Vogel J., Kiefer M., Mitchell-Olds T.. Evolution of the trnF(GAA) gene in Arabidopsis relatives and the Brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene.  Molecular Biology and Evolution. (2005);  22 1-12
• 59 Koch M., Dobeš C., Mitchell-Olds T.. Multiple hybrid formation in natural populations: concerted evolution of the internal transcribed spacer of nuclear ribosomal DNA (ITS) in North American Arabis divaricarpa (Brassicaceae).  Molecular Biology and Evolution. (2003 b);  20 338-350
• 60 Kress W. J., Wurdack K. J., Zimmer E. A., Weigt L. A., Janzen D. H.. Use of DNA barcodes to identify flowering plants.  Proceedings of the National Academy of Sciences of the USA. (2005);  102 8369-8374
• 61 Leach D. R. F.. Genetic Recombination. Oxford; Blackwell Science (1996): 1-192
• 62 Lee D., Grant A., Buchan D., Orengo Ch.. A structural perspective on genome evolution.  Current Opinion in Structural Biology. (2003);  13 359-369
• 63 Lee D. J., Blake T. K., Smith S. E.. Biparental inheritance of chloroplast DNA and the existence of heteroplasmic cells in alfalfa.  Theoretical and Applied Genetics. (1988);  76 545-549
• 64 Lemieux B., Turmel M., Lemieux C.. Unidirectional gene conversions in the chloroplast of Chlamydomonas interspecific hybrids.  Molecular and General Genetics. (1988);  212 48-55
• 65 Lemieux B., Turmel M., Lemieux C.. Recombination of Chlamydomonas chloroplast DNA occurs more frequently in the large inverted repeat sequence than in the single-copy regions.  Theoretical and Applied Genetics. (1990);  79 17-27
• 66 Lemieux C., Lee R. W.. Nonreciprocal recombination between alleles of the chloroplast 23S rRNA gene in interspecific Chlamydomonas crosses.  Proceedings of the National Academy of Sciences of the USA. (1987);  84 4166-4170
• 67 Lidholm J., Gustafsson P.. A three-step model for the rearrangement of the chloroplast trnK-psbA region of the gymnosperm Pinus contorta.  Nucleic Acids Research. (1991);  19 2881-2887
• 68 Lonsdale D. M., Brears T., Hodge T. P., Melville S. E., Rottmann W. H.. The plant mitochondrial genome: homologous recombination as a mechanism for generating heterogeneity.  Philosophical Transactions of the Royal Society London B. (1988);  319 149-163
• 69 Marshall Stark W., Boocock M. R., Sherratt D. J.. Catalysis by site-specific recombinases.  Trends in Genetics. (1992);  8 432-439
• 70 Martin W., Stroebe B., Goremykin V., Hansmann S., Hasegawa M., Kowallik K. V.. Gene transfer to the nucleus and the evolution of chloroplasts.  Nature. (1998);  393 162-165
• 71 McCabe P. F., Timmons A. M., Dix P. J.. A simple procedure for the isolation of streptomycin resistant plants in Solanaceae.  Molecular and General Genetics. (1989);  216 132-137
• 72 Medgyesy P., Fejes E., Maliga P.. Interspecific chloroplast recombination in a Nicotiana somatic hybrid.  Proceedings of the National Academy of Sciences of the USA. (1985);  82 6960-6964
• 73 Medgyesy P., Páy A., Márton L.. Transmission of paternal chloroplast in Nicotiana.  Molecular and General Genetics. (1986);  204 195-198
• 74 Morton B. R., Clegg M. T.. A chloroplast DNA mutational hotspot and gene conversion in a noncoding region near rbcL in the grass family (Poaceae).  Current Genetics. (1993);  24 357-365
• 75 Myers A. M., Grant D. M., Rabert D. K., Harris E. H., Boynton J. E., Gillham N. W.. Mutants of Chlamydomonas reinhardtii with physical alterations in their chloroplast DNA.  Plasmid. (1982);  7 133-151
• 76 Ogihara Y., Terachi T., Sasakuma T.. Intramolecular recombination of chloroplast genome mediated by short direct-repeat sequences in wheat species.  Proceedings of the National Academy of Sciences of the USA. (1988);  85 8573-8577
• 77 Ogihara Y., Terachi T., Sasakuma T.. Structural analysis of length mutations in a hot-spot region of wheat chloroplast DNAs.  Current Genetics. (1992);  22 251-258
• 78 Ogihara Y., Tsunewaki K.. Diversity and evolution of chloroplast DNA in Triticum and Aegilops as revealed by restriction-fragment analysis.  Theoretical and Applied Genetics. (1988);  76 321-332
• 79 Palmer J. D.. Comparative organization of chloroplast genomes.  Annual Review of Genetics. (1985);  19 325-354
• 80 Palmer J. D.. Plastid chromosomes: structure and evolution. Bogorad, L. and Vasil, I. K., eds. Cell Culture and Somatic Cell Genetics in Plants, Vol. 7, The Molecular Biology of Plastids. San Diego; Academic Press (1991): 5-53
• 81 Palmer J. D.. Mitochondrial DNA in plant systematics: applications and limitations. Soltis, P. S., Soltis, D. E., and Doyle, J. J., eds. Molecular Systematics of Plants. New York, London; Chapman and Hall (1992): 36-49
• 82 Podani J.. Multivariate Data Analysis in Ecology and Systematics. A Methodological Guide to the SYN‐TAX 5.0 Package. The Hague; SPB Academic Publishing (1994): 1-315
• 83 Prina A. R.. Mutator-induced cytoplasmic mutants in barley: genetic evidence of activation of a putative chloroplast transposon.  Journal of Heredity. (1996);  87 385-389
• 84 Quandt D., Müller K., Stech M., Frahm J.-P., Frey W., Hilu K. W., Borsch T.. Molecular evolution of the chloroplast trnL‐F region in land plants. Goffinet, B., Hollowell, V., and Magill, R., eds. Molecular Systematics of Bryophytes. Monographs in Systematic Botany from the Missouri Botanical Garden. (2004): 13-37
• 85 Reboud X., Zeyl C.. Organelle inheritance in plants.  Heredity. (1994);  72 132-140
• 86 Sang T., Crawford D. J., Stuessy T. F.. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae).  American Journal of Botany. (1997);  84 1120-1136
• 87 Santiago N., Herráiz C., Ramón Goni J., Messeguer X., Casacuberta J. M.. Genome-wide analysis of the emigrant family of MITEs of Arabidopsis thaliana.  Molecular Biology and Evolution. (2002);  19 2285-2293
• 88 Schaefer M. R., Kahn K.. Cyanobacterial transposons Tn5469 and Tn5541 represent a novel noncomposite transposon family.  Journal of Bacteriology. (1998);  180 6059-6063
• 89 Schmidt R.. Plant genome evolution: lessons from comparative genomics at the DNA level.  Plant Molecular Biology. (2002);  48 21-37
• 90 Schmitz U. K., Kowallik K. V.. Plastid inheritance in Epilobium.  Current Genetics. (1986);  11 1-5
• 91 Soltis D. E., Soltis P. S., Milligan B. G.. Intraspecific chloroplast DNA variation: systematic and phylogenetic implications. Soltis, P. S., Soltis, D. E., and Doyle, J. J., eds. Molecular Systematics of Plants. New York, London; Chapman and Hall (1992): 117-150
• 92 Stoike L. L., Sears B. B.. Plastome mutator-induced alterations arise in Oenothera chloroplast DNA through template slippage.  Genetics. (1998);  149 347-353
• 93 Swofford D. L.. Phylogenetic Anaylsis using Parsimony (and other methods). Version 4. Sunderlands, Massachusetts; Sinauer (2002): 1-144
• 94 Takaiwa F., Sugiura M.. Nucleotide sequence of the 16S - 23S spacer region in an rRNA gene cluster from tobacco chloroplast DNA.  Nucleic Acids Research. (1982);  10 2665-2676
• 95 Thanh N. D., Medgyesy P.. Limited chloroplast gene transfer via recombination overcomes plastome-genome incompatibility between Nicotiana tabacum and Solanum tuberosum.  Plant Molecular Biology. (1989);  12 87-93
• 96 Vijverberg K., Bachmann K.. Molecular evolution of a tandemly repeated trnF(GAA) gene in the chloroplast genomes of Microseris (Asteraceae) and the use of structural mutations in phylogenetic analyses.  Molecular Biology and Evolution. (1999);  16 1329-1340
• 97 Wittzell H.. Chloroplast DNA variation and reticulate evolution in sexual and apomictic sections of dandelions.  Molecular Ecology. (1999);  8 2023-2035
• 98 Wolfson R., Higgins K. G., Scars B. B.. Evidence for replication slippage in the evolution of Oenothera chloroplast DNA.  Molecular Biology and Evolution. (1991);  8 709-720
• 99 Zuker M.. On finding all suboptimal foldings of an RNA molecule.  Science. (1989);  244 48-52
• 100 Zuker M.. Mfold web server for nucleic acid folding and hybridization prediction.  Nucleic Acids Research. (2003);  31 3406-3415
• 101 Zurawski G., Clegg M. T., Brown A. D. H.. The nature of nucleotide sequence divergence betwen barley and maize chloroplast DNA.  Genetics. (1984);  106 735-749

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