Advertisement

Functional & Integrative Genomics

, Volume 11, Issue 4, pp 599–609 | Cite as

Recent insertion of a 52-kb mitochondrial DNA segment in the wheat lineage

  • Juncheng Zhang
  • Jizeng Jia
  • James Breen
  • Xiuying KongEmail author
Original Paper
  • 150 Downloads

Abstract

The assembly of a 1.3-Mb size region of the wheat genome has provided the opportunity to study a recent nuclear mitochondrial DNA insertion (NUMT). In the present study, we have studied two bacterial artificial chromosomes (BACs) and characterized a 52-kb NUMT segment from the tetraploid and hexaploid wheat BAC libraries. The conserved orthologous NUMT regions from tetraploid and hexaploid wheat Langdon and Chinese Spring shared identical gene haplotypes even though mutations (insertions, deletions, and substitutions) had occurred. The 52-kb NUMT was present in hexaploid variety Chinese Spring, but absent in variety Hope, by sequence comparison of their corresponding region. Amplifying the NUMT junctions using a set of the wheat materials including diploid, tetraploid, and hexaploid lines showed that none of the diploid wheat carried the region and only some tetraploid and hexaploid wheat were positive for the NUMT. Age estimation of the NUMT displayed the mean ages of Langdon NUMT and Chinese Spring NUMT to be 378,000 and 416,000 years ago, respectively. Reverse transcription PCR and sequencing of the nad7 gene showed 28 C → U RNA editing sites and four partial editing sites, as expected for mitochondrial DNA expression. Specific SNPs discriminated between cDNA from the nucleus and the mitochondria and suggested that the nuclear copy was not expressed. The mitochondrial DNA studied was inserted into the genome quite recently within the wheat lineage and gave rise to the non-coding nuclear nad7 gene. The NUMT segment could be lost and acquired frequently during the wheat evolution.

Keywords

Wheat NUMT nad7 gene RNA editing Evolution 

Notes

Acknowledgments

We thank Dr. Jing Wu for help in screening the high-density filters of tetraploid BAC library; Lingli Zheng, Lei Pan, and Guanhua Yang for their sequencing work; and Jiajie Wu and Qi Zuo for their sequence annotation assistance. The authors are grateful to Professor Rudi Appels for his contributions to the research in this manuscript. This research was supported by grants from the Ministry of Science and Technology of China (2006AA10A104) and Australia GRDC ET5.

Supplementary material

10142_2011_237_MOESM1_ESM.pdf (7 kb)
Supplementary Table S1 (PDF 7 kb)
10142_2011_237_MOESM2_ESM.pdf (8 kb)
Supplementary Table S2 (PDF 8 kb)
10142_2011_237_MOESM3_ESM.pdf (7 kb)
Supplementary Table S3 (PDF 7 kb)
10142_2011_237_MOESM4_ESM.pdf (8 kb)
Supplementary Table S4 (PDF 8 kb)
10142_2011_237_MOESM5_ESM.pdf (8 kb)
Supplementary Table S5 (PDF 7 kb)
10142_2011_237_MOESM6_ESM.pdf (92 kb)
Supplementary Table S6 (PDF 91 kb)
10142_2011_237_MOESM7_ESM.pdf (225 kb)
Supplementary Figure S1 Alignment of cDNA sequences of the nad7 gene. The left column represented the sequence names; the first three sequences were from mitochondria, Langdon, and Chinese Spring, respectively, which were manually spliced according to the gene annotation in the mitochondria genome by deleting the introns. The four sequences beginning with CS-cDNA were cDNA sequences from Chinese Spring; the letters following CS-cDNA represented the individual clones. Here, we only list the four representative sequences of the 16 sequenced clones due to limited space. Similarly, four sequences with names beginning with LDN-cDNA were nad7 cDNA sequences from Langdon. The sequences with the underlined black lines are the conserved primers used in the expression analysis. The vertical black lines represented the exon borders. The black arrows indicated the 28 C → U RNA editing sites, while the green arrows indicated the partial C → U RNA editing sites. The yellow quadrangle indicated the SNPs between NUMT and mitochondria of Langdon, and the yellow, double triangle, six-rayed star represented the SNPs between NUMT and mitochondria of Chinese Spring (PDF 224 kb)
10142_2011_237_MOESM8_ESM.pdf (534 kb)
Supplementary Figure S2 a Alignment of deletion sites in NUMT and mitochondrial region. Dashes indicate a 55-bp nucleotide fragment deletion. Black boxes indicate the target site duplication. b Chain slippage in replication of DNA resulting in the 55-bp nucleotide deletion. A and B indicated the two TTA direct repeats. The sequence between A and B is prone to form a stem-loop structure which could block the DNA polymerase combine with the DNA template (PDF 534 kb)
10142_2011_237_MOESM9_ESM.pdf (122 kb)
Supplementary Figure S3 a Schematic presentation of composition of wheat NUMT compared with the mitochondria. Red characters indicate the conserved rrn5–rrn18–trnfM three-gene cluster. b Generation and integration of wheat NUMT. “rrn5–rrn18–trnfM” haplotype of wheat NUMT originated from the recombination of the trnfM-1–nad1a and the rrn5–2-trnI haplotype of mitochondria meditated by IR repeat (copy 1 and copy 2; Ogihara et al. 2005) (PDF 121 kb)

References

  1. Adams KL, Rosenblueth M, Qiu YL, Palmer JD (2001) Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. Genetics 158:1289–1300PubMedGoogle Scholar
  2. Andre C, Levy A, Walbot V (1992) Small repeated sequences and the structure of plant mitochondrial genomes. Trends Genet 8:128–132PubMedGoogle Scholar
  3. Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Report 9:208–218CrossRefGoogle Scholar
  4. Behura SK (2007) Analysis of nuclear copies of mitochondrial sequences in honeybee (Apis mellifera) genome. Mol Biol Evol 24:1492–1505PubMedCrossRefGoogle Scholar
  5. Bendich AJ (1996) Structural analysis of mitochondrial DNA molecules from fungi and plants using moving pictures and pulsed-field gel electrophoresis. J Mol Biol 255:564–588PubMedCrossRefGoogle Scholar
  6. Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:29–36PubMedCrossRefGoogle Scholar
  7. Bennetzen JL, Ma J, Devos KM (2005) Mechanisms of recent genome size variation in flowering plants. Ann Bot 95:127–132PubMedCrossRefGoogle Scholar
  8. Bonen L (2006) Mitochondrial genes leave home. New Phytol 172:379–381PubMedCrossRefGoogle Scholar
  9. Bonen L, Williams K, Bird S, Wood C (1994) The NADH dehydrogenase subunit 7 gene is interrupted by four group II introns in the wheat mitochondrial genome. Mol Gen Genet 244:81–89PubMedCrossRefGoogle Scholar
  10. Breen J, Li D, Dunn DS, Bekes F, Kong X, Zhang J, Jia J, Wicker T, Mago R, Ma W, Bellgard M, Appels R (2010) Wheat beta-expansin (EXPB11) genes: identification of the expressed gene on chromosome 3BS carrying a pollen allergen domain. BMC Plant Biol 10:99PubMedCrossRefGoogle Scholar
  11. Cenci A, Chantret N, Kong X, Gu Y, Anderson OD, Fahima T, Distelfeld A, Dubcovsky J (2003) Construction and characterization of a half million clone BAC library of durum wheat (Triticum turgidum ssp. durum). Theor Appl Genet 107:931–939PubMedCrossRefGoogle Scholar
  12. Chantret N, Salse J, Sabot F, Rahman S, Bellec A, Laubin B, Dubois I, Dossat C, Sourdille P, Joudrier P, Gautier MF, Cattolico L, Beckert M, Aubourg S, Weissenbach J, Caboche M, Bernard M, Leroy P, Chalhoub B (2005) Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17:1033–1045PubMedCrossRefGoogle Scholar
  13. Charles M, Belcram H, Just J, Huneau C, Viollet A, Couloux A, Segurens B, Carter M, Huteau V, Coriton O, Appels R, Samain S, Chalhoub B (2008) Dynamics and differential proliferation of transposable elements during the evolution of the B and A genomes of wheat. Genetics 180:1071–1086PubMedCrossRefGoogle Scholar
  14. Deutsch M, Long M (1999) Intron–exon structures of eukaryotic model organisms. Nucleic Acids Res 27:3219–3228PubMedCrossRefGoogle Scholar
  15. Devos KM, Brown JK, Bennetzen JL (2002) Genome size reduction through illegitimate recombination counteracts genome expansion in Arabidopsis. Genome Res 12:1075–1079PubMedCrossRefGoogle Scholar
  16. Grohmann L, Brennicke A, Schuster W (1992) The mitochondrial gene encoding ribosomal protein S12 has been translocated to the nuclear genome in Oenothera. Nucleic Acids Res 20:5641–5646PubMedCrossRefGoogle Scholar
  17. Groth-Malonek M, Wahrmund U, Polsakiewicz M, Knoop V (2007) Evolution of a pseudogene: exclusive survival of a functional mitochondrial nad7 gene supports Haplomitrium as the earliest liverwort lineage and proposes a secondary loss of RNA editing in Marchantiidae. Mol Biol Evol 24:1068–1074PubMedCrossRefGoogle Scholar
  18. Hazkani-Covo E, Graur D (2007) A comparative analysis of numt evolution in human and chimpanzee. Mol Biol Evol 24:13–18PubMedCrossRefGoogle Scholar
  19. Huang CY, Grunheit N, Ahmadinejad N, Timmis JN, Martin W (2005) Mutational decay and age of chloroplast and mitochondrial genomes transferred recently to angiosperm nuclear chromosomes. Plant Physiol 138:1723–1733PubMedCrossRefGoogle Scholar
  20. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110:462–467PubMedCrossRefGoogle Scholar
  21. Kirik A, Salomon S, Puchta H (2000) Species-specific double-strand break repair and genome evolution in plants. EMBO J 19:5562–5566PubMedCrossRefGoogle Scholar
  22. Klein M, Eckert-Ossenkopp U, Schmiedeberg I, Brandt P, Unseld M, Brennicke A, Schuster W (1994) Physical mapping of the mitochondrial genome of Arabidopsis thaliana by cosmid and YAC clones. Plant J 6:447–455PubMedCrossRefGoogle Scholar
  23. Kleine T, Maier UG, Leister D (2009) DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 60:115–138PubMedCrossRefGoogle Scholar
  24. Kong XY, Gu YQ, You FM, Dubcovsky J, Anderson OD (2004) Dynamics of the evolution of orthologous and paralogous portions of a complex locus region in two genomes of allopolyploid wheat. Plant Mol Biol 54:55–69PubMedCrossRefGoogle Scholar
  25. Kota R, Spielmeyer W, McIntosh RA, Lagudah ES (2006) Fine genetic mapping fails to dissociate durable stem rust resistance gene Sr2 from pseudo-black chaff in common wheat (Triticum aestivum L.). Theor Appl Genet 112:492–499PubMedCrossRefGoogle Scholar
  26. Krumsiek J, Arnold R, Rattei T (2007) Gepard: a rapid and sensitive tool for creating dotplots on genome scale. Bioinformatics 23:1026–1028PubMedCrossRefGoogle Scholar
  27. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163PubMedCrossRefGoogle Scholar
  28. Leister D (2005) Origin, evolution and genetic effects of nuclear insertions of organelle DNA. Trends Genet 21:655–663PubMedCrossRefGoogle Scholar
  29. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860–869PubMedCrossRefGoogle Scholar
  30. Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci USA 100:8612–8614PubMedCrossRefGoogle Scholar
  31. Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17PubMedCrossRefGoogle Scholar
  32. Matsuo M, Ito Y, Yamauchi R, Obokata J (2005) The rice nuclear genome continuously integrates, shuffles, and eliminates the chloroplast genome to cause chloroplast–nuclear DNA flux. Plant Cell 17:665–675PubMedCrossRefGoogle Scholar
  33. Mishmar D, Ruiz-Pesini E, Brandon M, Wallace DC (2004) Mitochondrial DNA-like sequences in the nucleus (NUMTs): insights into our African origins and the mechanism of foreign DNA integration. Hum Mutat 23:125–133PubMedCrossRefGoogle Scholar
  34. Noutsos C, Richly E, Leister D (2005) Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants. Genome Res 15:616–628PubMedCrossRefGoogle Scholar
  35. Ogihara Y, Yamazaki Y, Murai K, Kanno A, Terachi T, Shiina T, Miyashita N, Nasuda S, Nakamura C, Mori N, Takumi S, Murata M, Futo S, Tsunewaki K (2005) Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res 33:6235–6250PubMedCrossRefGoogle Scholar
  36. Ouyang S, Buell CR (2004) The TIGR Plant Repeat Databases: a collective resource for the identification of repetitive sequences in plants. Nucleic Acids Res 32:D360–363PubMedCrossRefGoogle Scholar
  37. Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Berges H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104PubMedCrossRefGoogle Scholar
  38. Richly E, Leister D (2004a) NUMTs in sequenced eukaryotic genomes. Mol Biol Evol 21:1081–1084PubMedCrossRefGoogle Scholar
  39. Richly E, Leister D (2004b) NUPTs in sequenced eukaryotes and their genomic organization in relation to NUMTs. Mol Biol Evol 21:1972–1980PubMedCrossRefGoogle Scholar
  40. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  41. Smith DB, Flavell RB (1975) Characterisation of the wheat genome by renaturation kinetics. Chromosoma 50:223–242CrossRefGoogle Scholar
  42. Song R, Llaca V, Messing J (2002) Mosaic organization of orthologous sequences in grass genomes. Genome Res 12:1549–1555PubMedCrossRefGoogle Scholar
  43. Stupar RM, Lilly JW, Town CD, Cheng Z, Kaul S, Buell CR, Jiang J (2001) Complex mtDNA constitutes an approximate 620-kb insertion on Arabidopsis thaliana chromosome 2: implication of potential sequencing errors caused by large-unit repeats. Proc Natl Acad Sci USA 98:5099–5103PubMedCrossRefGoogle Scholar
  44. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135PubMedCrossRefGoogle Scholar
  45. Unseld M, Marienfeld JR, Brandt P, Brennicke A (1997) The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet 15:57–61PubMedCrossRefGoogle Scholar
  46. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249PubMedCrossRefGoogle Scholar
  47. Wicker T, Stein N, Albar L, Feuillet C, Schlagenhauf E, Keller B (2001) Analysis of a contiguous 211 kb sequence in diploid wheat (Triticum monococcum L.) reveals multiple mechanisms of genome evolution. Plant J 26:307–316PubMedCrossRefGoogle Scholar
  48. Woischnik M, Moraes CT (2002) Pattern of organization of human mitochondrial pseudogenes in the nuclear genome. Genome Res 12:885–893PubMedGoogle Scholar
  49. Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058PubMedCrossRefGoogle Scholar
  50. Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298CrossRefGoogle Scholar
  51. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Juncheng Zhang
    • 1
  • Jizeng Jia
    • 1
  • James Breen
    • 2
  • Xiuying Kong
    • 1
    • 3
    Email author
  1. 1.Key Laboratory of Crop Germplasm Resources and Utilization, MOA/Institute of Crop Science, CAAS/The Key Facility for Crop Gene Resources and Genetic ImprovementBeijingPeople’s Republic of China
  2. 2.Centre for Comparative GenomicsMurdoch UniversityMurdochAustralia
  3. 3.Institute of Crop Science, Chinese Academy of Agricultural SciencesBeijingPeople’s Republic of China

Personalised recommendations