Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber

Plant Cell

Volumn 23, Issue 7, 2011, Pages 2499-2513

  Alverson, Andrew J ^a   Rice, Danny W ^a   Dickinson, Stephanie ^a   Barry, Kerrie ^b   Palmer, Jeffrey D ^a  

^a INDIANA UNIVERSITY   (United States)

^b DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CUCUMIS SATIVUS; CUCURBITACEAE; MAGNOLIOPHYTA;

EID: 80051930449     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.111.087189     Document Type: Article

References (77)

1. Adams, K.L., Qiu, Y.-L., Stoutemyer, M., and Palmer, J.D. (2002). Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc. Natl. Acad. Sci. USA 99: 9905-9912.
2. Allen, J.O., et al. (2007). Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 177: 1173-1192.
3. Alverson, A.J., Wei, X.X., Rice, D.W., Stern, D.B., Barry, K., and Palmer, J.D. (2010). Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol. Biol. Evol. 27: 1436-1448.
4. Alverson, A.J., Zhuo, S., Rice, D.W., Sloan, D.B., and Palmer, J.D. (2011). The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS ONE 6: e16404.
5. Armstrong, M.R., Blok, V.C., and Phillips, M.S. (2000). A multipartite mitochondrial genome in the potato cyst nematode Globodera pallida. Genetics 154: 181-192.
6. Arrieta-Montiel, M.P., Shedge, V., Davila, J., Christensen, A.C., and Mackenzie, S.A. (2009). Diversity of the Arabidopsis mitochondrial genome occurs via nuclear-controlled recombination activity. Genetics 183: 1261-1268.
7. Backert, S., and Bö rner, T. (2000). Phage T4-like intermediates of DNA replication and recombination in the mitochondria of the higher plant Chenopodium album (L.). Curr. Genet. 37: 304-314.
8. Backert, S., Lynn Nielsen, B., and Börner, T. (1997). The mystery of the rings: Structure and replication of mitochondrial genomes from higher plants. Trends Plant Sci. 2: 477-483.
9. Bartoszewski, G., Gawronski, P., Szklarczyk, M., Verbakel, H., and Havey, M.J. (2009). A one-megabase physical map provides insights on gene organization in the enormous mitochondrial genome of cucumber. Genome 52: 299-307.
10. Bell, C.D., Soltis, D.E., and Soltis, P.S. (2010). The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97: 1296-1303.
11. Bendich, A.J. (1993). Reaching for the ring: The study of mitochondrial genome structure. Curr. Genet. 24: 279-290.
12. Bock, R. (2010). The give-and-take of DNA: Horizontal gene transfer in plants. Trends Plant Sci. 15: 11-22.
13. Bucka, A., and Stasiak, A. (2001). RecA-mediated strand exchange traverses substitutional heterologies more easily than deletions or insertions. Nucleic Acids Res. 29: 2464-2470.
14. Burger, G., Forget, L., Zhu, Y., Gray, M.W., and Lang, B.F. (2003). Unique mitochondrial genome architecture in unicellular relatives of animals. Proc. Natl. Acad. Sci. USA 100: 892-897.
15. Burger, G., and Lang, B.F. (2003). Parallels in genome evolution in mitochondria and bacterial symbionts. IUBMB Life 55: 205-212.
16. Coulthart, M.B., Huh, G.S., and Gray, M.W. (1990). Physical organization of the 18S and 5S ribosomal RNA genes in the mitochondrial genome of rye (Secale cereale L.). Curr. Genet. 17: 339-346.
17. Folkerts, O., and Hanson, M.R. (1989). Three copies of a single recombination repeat occur on the 443 kb master circle of the Petunia hybrida 3704 mitochondrial genome. Nucleic Acids Res. 17: 7345-7357.
18. Goremykin, V.V., Salamini, F., Velasco, R., and Viola, R. (2009). Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol. Biol. Evol. 26: 99-110.
19. Grewe, F., Viehoever, P., Weisshaar, B., and Knoop, V. (2009). A trans-splicing group I intron and tRNA-hyperediting in the mitochondrial genome of the lycophyte Isoetes engelmannii. Nucleic Acids Res. 37: 5093-5104.
20. Havey, M.J., McCreight, J.D., Rhodes, B., and Taurick, G. (1998). Differential transmission of the Cucumis organellar genomes. Theor. Appl. Genet. 97: 122-128.
21. Hazkani-Covo, E., Sorek, R., and Graur, D. (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.
22. Hazkani-Covo, E., Zeller, R.M., and Martin, W. (2010). Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genet. 6: e1000834.
23. Huang, S., et al. (2009). The genome of the cucumber, Cucumis sativus L. Nat. Genet. 41: 1275-1281.
24. Inbar, O., Liefshitz, B., Bitan, G., and Kupiec, M. (2000). The relationship between homology length and crossing over during the repair of a broken chromosome. J. Biol. Chem. 275: 30833-30838.
25. Jurka, J. (2000). Repbase update: A database and an electronic journal of repetitive elements. Trends Genet. 16: 418-420.
26. Kim, J.S., Jung, J.D., Lee, J.A., Park, H.W., Oh, K.H., Jeong, W.J., Choi, D.W., Liu, J.R., and Cho, K.Y. (2006). Complete sequence and organization of the cucumber (Cucumis sativus L. cv. Baekmibaekdadagi) chloroplast genome. Plant Cell Rep. 25: 334-340.
27. King, S.R., and Richardson, J.P. (1986). Role of homology and pathway specificity for recombination between plasmids and bacteriophage lambda. Mol. Gen. Genet. 204: 141-147.
28. Knoop, V., Unseld, M., Marienfeld, J., Brandt, P., Sü nkel, S., Ullrich, H., and Brennicke, A. (1996). copia-, gypsy-and LINE-like retrotransposon fragments in the mitochondrial genome of Arabidopsis thaliana. Genetics 142: 579-585.
29. Kolodner, R., and Tewari, K.K. (1972). Physicochemical characterization of mitochondrial DNA from pea leaves. Proc. Natl. Acad. Sci. USA 69: 1830-1834.
30. Korbel, J.O., et al. (2007). Paired-end mapping reveals extensive structural variation in the human genome. Science 318: 420-426.
31. Kubo, T., Nishizawa, S., Sugawara, A., Itchoda, N., Estiati, A., and Mikami, T. (2000). The complete nucleotide sequence of the mitochondrial genome of sugar beet (Beta vulgaris L.) reveals a novel gene for tRNA(Cys)(GCA). Nucleic Acids Res. 28: 2571-2576.
32. Ladoukakis, E.D., Theologidis, I., Rodakis, G.C., and Zouros, E. (2011). Homologous recombination between highly diverged mitochondrial sequences: Examples from maternally and paternally transmitted genomes. Mol. Biol. Evol. 28: 1847-1859.
33. Lejeune, B., Delorme, S., Delcher, E., and Quetier, F. (1987). Recombination in wheat mitochondrial DNA: Occurrence of nine different genomic contexts for the 18 S-5 S genes. Plant Physiol. Biochem. 25: 227-233.
34. Lilly, J.W., and Havey, M.J. (2001). Small, repetitive DNAs contribute significantly to the expanded mitochondrial genome of cucumber. Genetics 159: 317-328.
35. Lonsdale, D.M., and Grienenberger, J.M. (1992). The mitochondrial genome of plants. In Cell Organelles, R.G. Herrmann, ed (Vienna, Austria: Springer-Verlag), pp. 183-218.
36. Lonsdale, D.M., Hodge, T.P., and Fauron, C.M. (1984). The physical map and organisation of the mitochondrial genome from the fertile cytoplasm of maize. Nucleic Acids Res. 12: 9249-9261.
37. Lopez, J.V., Yuhki, N., Masuda, R., Modi, W., and O'Brien, S.J. (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.
38. Lough, A.N., Roark, L.M., Kato, A., Ream, T.S., Lamb, J.C., Birchler, J.A., and Newton, K.J. (2008). Mitochondrial DNA transfer to the nucleus generates extensive insertion site variation in maize. Genetics 178: 47-55.
39. Lukes, J., Hashimi, H., and Źková, A. (2005). Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr. Genet. 48: 277-299.
40. Makizumi, Y., Igarashi, M., Gotoh, K., Murao, K., Yamamoto, M., Udonsri, N., Ochiai, H., Thummabenjapone, P., and Kaku, H. (2011). Genetic diversity and pathogenicity of cucurbit-associated Acidovorax. J. Gen. Plant Pathol. 77: 24-32.
41. Maréchal, A., and Brisson, N. (2010). Recombination and the maintenance of plant organelle genome stability. New Phytol. 186: 299-317.
42. Martin, H.L., O'Brien, R.G., and Abbott, D.V. (1999). First report of Acidovorax avenae subsp. citrulli as a pathogen of cucumber. Plant Dis. 83: 965-965.
43. Nakazato, T., and Gastony, G.J. (2006). High-throughput RFLP genotyping method for large genomes based on a chemiluminescent detection system. Plant Mol. Biol. Rep. 24: 245a-245f.
44. Notsu, Y., Masood, S., Nishikawa, T., Kubo, N., Akiduki, G., Nakazono, M., Hirai, A., and Kadowaki, K. (2002). The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: Frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol. Genet. Genomics 268: 434-445.
45. Oldenburg, D.J., and Bendich, A.J. (1996). Size and structure of replicating mitochondrial DNA in cultured tobacco cells. Plant Cell 8: 447-461.
46. Oldenburg, D.J., and Bendich, A.J. (2001). Mitochondrial DNA from the liverwort Marchantia polymorpha: circularly permuted linear molecules, head-to-tail concatemers, and a 59 protein. J. Mol. Biol. 310: 549-562.
47. Palmer, J.D. (1982). Physical and gene mapping of chloroplast DNA from Atriplex triangularis and Cucumis sativa. Nucleic Acids Res. 10: 1593-1605.
48. Palmer, J.D. (1988). Intraspecific variation and multicircularity in Brassica mitochondrial DNAs. Genetics 118: 341-351.
49. Palmer, J.D., and Herbon, L.A. (1986). Tricircular mitochondrial genomes of Brassica and Raphanus: Reversal of repeat configurations by inversion. Nucleic Acids Res. 14: 9755-9764.
50. Palmer, J.D., and Herbon, L.A. (1987). Unicircular structure of the Brassica hirta mitochondrial genome. Curr. Genet. 11: 565-570.
51. Palmer, J.D., and Shields, C.R. (1984). Tripartite structure of the Brassica campestris mitochondrial genome. Nature 307: 437-440.
52. Pollard, V.W., Rohrer, S.P., Michelotti, E.F., Hancock, K., and Hajduk, S.L. (1990). Organization of minicircle genes for guide RNAs in Trypanosoma brucei. Cell 63: 783-790.
53. Qiu, Y.-L., Cho, Y.R., Cox, J.C., and Palmer, J.D. (1998). The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671-674.
54. Richly, E., and Leister, D. (2004). NUPTs in sequenced eukaryotesand their genomic organization in relation to NUMTs. Mol. Biol. Evol. 21: 1972-1980.
55. Richly, E., and Leister, D. (2004). NUMTs in sequenced eukaryotic genomes. Mol. Biol. Evol. 21: 1081-1084.
56. Roark, L.M., Hui, A.Y., Donnelly, L., Birchler, J.A., and Newton, K.J. (2010). Recent and frequent insertions of chloroplast DNA into maize nuclear chromosomes. Cytogenet. Genome Res. 129: 17-23.
57. Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual, 3rd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
58. Sanchez-Puerta, M.V., Cho, Y., Mower, J.P., Alverson, A.J., and Palmer, J.D. (2008). Frequent, phylogenetically local horizontal transfer of the cox1 group I Intron in flowering plant mitochondria. Mol. Biol. Evol. 25: 1762-1777.
59. Satoh, M., Kubo, T., Nishizawa, S., Estiati, A., Itchoda, N., and Mikami, T. (2004). The cytoplasmic male-sterile type and normal type mitochondrial genomes of sugar beet share the same complement of genes of known function but differ in the content of expressed ORFs. Mol. Genet. Genomics 272: 247-256.
60. Schaefer, H., Heibl, C., and Renner, S.S. (2009). Gourds afloat: A dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc. Biol. Sci. 276: 843-851.
61. Shao, R.F., Kirkness, E.F., and Barker, S.C. (2009). The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus. Genome Res. 19: 904-912.
62. Shedge, V., Arrieta-Montiel, M., Christensen, A.C., and Mackenzie, S.A. (2007). Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19: 1251-1264.
63. Shen, P., and Huang, H.V. (1986). Homologous recombination in Escherichia coli: Dependence on substrate length and homology. Genetics 112: 441-457.
64. Siculella, L., Damiano, F., Cortese, M.R., Dassisti, E., Rainaldi, G., Gallerani, R., and De Benedetto, C. (2001). Gene content and organization of the oat mitochondrial genome. Theor. Appl. Genet. 103: 359-365.
65. Siculella, L., and Palmer, J.D. (1988). Physical and gene organization of mitochondrial DNA in fertile and male sterile sunflower. CMSassociated alterations in structure and transcription of the atpA gene. Nucleic Acids Res. 16: 3787-3799.
66. Sloan, D.B., Alverson, A.J., Storchová, H., Palmer, J.D., and Taylor, D.R. (2010). Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol. Biol. 10: 274.
67. Small, I.D., Isaac, P.G., and Leaver, C.J. (1987). Stoichiometric differences in DNA molecules containing the atpA gene suggest mechanisms for the generation of mitochondrial genome diversity in maize. EMBO J. 6: 865-869.
68. Stern, D.B., and Lonsdale, D.M. (1982). Mitochondrial and chloroplast genomes of maize have a 12-kilobase DNA sequence in common. Nature 299: 698-702.
69. Stern, D.B., and Newton, K.J. (1985). Mitochondrial gene expression in Cucurbitaceae: Conserved and variable features. Curr. Genet. 9: 395-404.
70. Stern, D.B., and Palmer, J.D. (1986). Tripartite mitochondrial genome of spinach: Physical structure, mitochondrial gene mapping, and locations of transposed chloroplast DNA sequences. Nucleic Acids Res. 14: 5651-5666.
71. Stern, D.B., Palmer, J.D., Thompson, W.F., and Lonsdale, D.M. (1983). Mitochondrial DNA sequence evolution and homology to chloroplast DNA in angiosperms. In Plant Molecular Biology, ICNUCLA Symposia on Molecular and Cellular Biology, R.B. Goldberg, ed (New York: Alan R. Liss), pp. 467-477.
72. Sturm, N.R., and Simpson, L. (1990). Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit III mRNA. Cell 61: 879-884.
73. Takemura, M., Oda, K., Yamato, K., Ohta, E., Nakamura, Y., Nozato, N., Akashi, K., and Ohyama, K. (1992). Gene clusters for ribosomal proteins in the mitochondrial genome of a liverwort, Marchantia polymorpha. Nucleic Acids Res. 20: 3199-3205.
74. Vlcek, C., Marande, W., Teijeiro, S., Lukes, J., and Burger, G. (2011). Systematically fragmented genes in a multipartite mitochondrial genome. Nucleic Acids Res. 39: 979-988.
75. Ward, B.L., Anderson, R.S., and Bendich, A.J. (1981). The mitochondrial genome is large and variable in a family of plants (cucurbitaceae). Cell 25: 793-803.
76. Watanabe, K.I., Bessho, Y., Kawasaki, M., and Hori, H. (1999). Mitochondrial genes are found on minicircle DNA molecules in the mesozoan animal Dicyema. J. Mol. Biol. 286: 645-650.
77. Zhang, Z.D., Green, B.R., and Cavalier-Smith, T. (1999). Single gene circles in dinoflagellate chloroplast genomes. Nature 400: 155-159.