De novo assembly of the carrot mitochondrial genome using next generation sequencing of whole genomic DNA provides first evidence of DNA transfer into an angiosperm plastid genome

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Iorizzo, Massimo ^a   Senalik, Douglas ^a   Szklarczyk, Marek ^b   Grzebelus, Dariusz ^b   Spooner, David ^a   Simon, Philipp ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

Author keywords

Assembly structure visualization; Daucus carota; De novo assembly; Intercompartmental DNA transfer; Mitochondrial genome; Next generation sequencing; Plastid genome

Indexed keywords

APIACEAE; DAUCUS; DAUCUS CAROTA; EMBRYOPHYTA; MAGNOLIOPHYTA; TRACHEOPHYTA;

PLANT DNA;

ANGIOSPERM; ARTICLE; CARROT; EVALUATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HORIZONTAL GENE TRANSFER; METHODOLOGY; MITOCHONDRIAL GENOME; MOLECULAR GENETICS; PLANT GENOME;

ANGIOSPERMS; DAUCUS CAROTA; DNA, PLANT; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; GENOME, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA;

EID: 84862230226     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-61     Document Type: Article

References (70)

1. Kubo T, Newton KJ. Angiosperm mitochondrial genomes and mutations. Mitochondrion 2008, 8:5-14. 10.1016/j.mito.2007.10.006, 18065297.
2. Kubo T, Mikami T. Organization and variation of angiosperm mitochondrial genome. Physiol Plantarum 2007, 129:6-13.
3. Richardson AO, Palmer JD. Horizontal gene transfer in plants. J Exp Bot 2007, 58:1-9.
4. Archibald J, Richards T. Gene transfer: anything goes in plant mitochondria. BMC Biol 2010, 8:147. 10.1186/1741-7007-8-147, 3008690, 21176244.
5. Goremykin VV, Salamini F, Velasco R, Viola R. Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 2009, 26:99-110.
6. Mower J, Stefanovic S, Hao W, Gummow J, Jain K, Ahmed D, Palmer J. Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 2010, 8(1):150. 10.1186/1741-7007-8-150, 3022774, 21176201.
7. 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. Structural dynamics of cereal mitochondrial genomes as revealed by complete nucleotide sequencing of the wheat mitochondrial genome. Nucleic Acids Res 2005, 33:6235-6250. 10.1093/nar/gki925, 1275586, 16260473.
8. Chang S, Yang T, Du T, Huang Y, Chen J, Yan J, He J, Guan R. Mitochondrial genome sequencing helps show the evolutionary mechanism of mitochondrial genome formation in Brassica. BMC Genomics 2011, 12:497. 10.1186/1471-2164-12-497, 3204307, 21988783.
9. Allen JO, Fauron CM, Minx P, Roark L, Oddiraju S, Lin GN, Meyer L, Sun H, Kim K, Wang C, Du F, Xu D, Gibson M, Cifrese J, Clifton SW, Newton KJ. Comparisons among two fertile and three male-sterile mitochondrial genomes of maize. Genetics 2007, 177:1173-1192. 10.1534/genetics.107.073312, 2034622, 17660568.
10. Alverson AJ, Wei X, Rice DW, Stern DB, Barry K, Palmer JD. Insights into the Evolution of Mitochondrial Genome Size from Complete Sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 2010, 27:1436-1448. 10.1093/molbev/msq029, 2877997, 20118192.
11. Woodson JD, Chory J. Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 2008, 9:383-395. 10.1038/nrg2348, 18368053.
12. Wolf JB. Cytonuclear interactions can favor the evolution of genomic imprinting. Evolution 2009, 63:1364-1371. 10.1111/j.1558-5646.2009.00632.x, 19425202.
13. Kleine T, Maier UG, Leister D. DNA transfer from organelles to the nucleus: the idiosyncratic genetics of endosymbiosis. Annu Rev Plant Biol 2009, 60:115-138. 10.1146/annurev.arplant.043008.092119, 19014347.
14. Smith DR. Extending the limited transfer window hypothesis to inter-organelle DNA migration. Genome Biol Evol 2011, 3:743-748. 10.1093/gbe/evr068, 3163470, 21803764.
15. Jex AR, Hall RS, Littlewood DT, Gasser RB. An integrated pipeline for next-generation sequencing and annotation of mitochondrial genomes. Nucleic Acids Res 2010, 38:522-533. 10.1093/nar/gkp883, 2811008, 19892826.
16. Webb KM, Rosenthal BM. Next-generation sequencing of the Trichinella murrelli mitochondrial genome allows comprehensive comparison of its divergence from the principal agent of human trichinellosis, Trichinella spiralis. Infect Genet Evol 2011, 11:116-123. 10.1016/j.meegid.2010.10.001, 20946970.
17. Gunnarsdóttir ED, Li M, Bauchet M, Finstermeier K, Stoneking M. High-throughput sequencing of complete human mtDNA genomes from the Philippines. Genome Res 2011, 21:1-11. 10.1101/gr.107615.110, 3012916, 21147912.
18. Cui Z, Liu Y, Li CP, You F, Chu KH. The complete mitochondrial genome of the large yellow croaker, Larimichthys crocea (Perciformes, Sciaenidae): Unusual features of its control region and the phylogenetic position of the Sciaenidae. Gene 2009, 432:33-43. 10.1016/j.gene.2008.11.024, 19100818.
19. Yang M, Zhang X, Liu G, Yin Y, Chen K, Yun Q, Zhao D, Al-Mssallem IS, Yu J. The complete chloroplast genome sequence of date palm (Phoenix dactylifera L.). PLoS One 2010, 5:e12762. 10.1371/journal.pone.0012762, 2939885, 20856810.
20. Tangphatsornruang S, Sangsrakru D, Chanprasert J, Uthaipaisanwong P, Yoocha T, Jomchai N, Tragoonrung S. The chloroplast genome sequence of mungbean (Vigna radiata) determined by high-throughput pyrosequencing: structural organization and phylogenetic relationships. DNA Res 2010, 17:11-22. 10.1093/dnares/dsp025, 2818187, 20007682.
21. Nock CJ, Waters DL, Edwards MA, Bowen SG, Rice N, Cordeiro GM, Henry RJ. Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol J 2011, 9:328-333. 10.1111/j.1467-7652.2010.00558.x, 20796245.
22. Straub SC, Fishbein M, Livshultz T, Foster Z, Parks M, Weitemier K, Cronn RC, Liston A. Building a model: developing genomic resources for common milkweed (Asclepias syriaca) with low coverage genome sequencing. BMC Genomics 2011, 12:211. 10.1186/1471-2164-12-211, 3116503, 21542930.
23. Lassmann T, Sonnhammer EL. Kalign-an accurate and fast multiple sequence alignment algorithm. BMC Bioinforma 2005, 6:298.
24. Ruhlman T, Lee SB, Jansen RK, Hostetler JB, Tallon LJ, Town CD, Daniell H. Complete plastid genome sequence of Daucus carota: implications for biotechnology and phylogeny of angiosperms. BMC Genomics 2006, 7:222. 10.1186/1471-2164-7-222, 1579219, 16945140.
25. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen Z, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer ML, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu P, Begley RF, Rothberg JM. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380. 1464427, 16056220.
26. Clement NL, Snell Q, Clement MJ, Hollenhorst PC, Purwar J, Graves BJ, Cairns BR, Johnson WE. The GNUMAP algorithm: unbiased probabilistic mapping of oligonucleotides from next-generation sequencing. Bioinformatics 2010, 26:38-45. 10.1093/bioinformatics/btp614, 19861355.
27. Rodriguez-Moreno L, Gonzalez VM, Benjak A, Marti MC, Puigdomenech P, Aranda MA, Garcia-Mas J. Determination of the melon chloroplast and mitochondrial genome sequences reveals that the largest reported mitochondrial genome in plants contains a significant amount of DNA having a nuclear origin. BMC Genomics 2011, 12:424. 10.1186/1471-2164-12-424, 3175227, 21854637.
28. Alverson AJ, Zhuo S, Rice DW, Sloan DB, Palmer JD. The mitochondrial genome of the legume Vigna radiata and the analysis of recombination across short mitochondrial repeats. PLoS One 2011, 6:e16404. 10.1371/journal.pone.0016404, 3024419, 21283772.
29. Bach I, Olesen A, Simon P. PCR-based markers to differentiate the mitochondrial genomes of petaloid and male fertile carrot (Daucus carota L.). Euphytica 2002, 127:353-365.
30. Szklarczyk M, Oczkowski M, Augustyniak H, Börner T, Linke B, Michalik B. Organisation and expression of mitochondrial atp9 genes from CMS and fertile carrots. Theor Appl Genet 2000, 100(2):263-270.
31. Macas J, Neumann P, Navratilova A. Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago truncatula. BMC Genomics 2007, 8:427. 10.1186/1471-2164-8-427, 2206039, 18031571.
32. Tangphatsornruang S, Somta P, Uthaipaisanwong P, Chanprasert J, Sangsrakru D, Seehalak W, Sommanas W, Tragoonrung S, Srinives P. Characterization of microsatellites and gene contents from genome shotgun sequences of mungbean (Vigna radiata (L.) Wilczek). BMC Plant Biol 2009, 9:137. 10.1186/1471-2229-9-137, 2788553, 19930676.
33. Zhu H, Senalik D, McCown BH, Zeldin EL, Speers J, Hyman J, Bassil N, Hummer K, Simon PW, Zalapa JE. Mining and validation of pyrosequenced simple sequence repeats (SSRs) from American cranberry (Vaccinium macrocarpon Ait.). Theor Appl Genet,in press.
34. Lutz KA, Wang W, Zdepski A, Michael TP. Isolation and analysis of high quality nuclear DNA with reduced organellar DNA for plant genome sequencing and resequencing. BMC Biotechnol 2011, 11:54. 10.1186/1472-6750-11-54, 3131251, 21599914.
35. Aird D, Ross MG, Chen WS, Danielsson M, Fennell T, Russ C, Jaffe DB, Nusbaum C, Gnirke A. Analyzing and minimizing PCR amplification bias in Illumina sequencing libraries. Genome Biol 2011, 12:R18. 10.1186/gb-2011-12-2-r18, 3188800, 21338519.
36. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D. Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Res 2008, 18:2024-2033. 10.1101/gr.080200.108, 2593571, 18818371.
37. Nielsen CB, Cantor M, Dubchak I, Gordon D, Wang T. Visualizing genomes: techniques and challenges. Nat Methods 2010, 7(Suppl 3):S5-S15.
38. Cahill MJ, Koser CU, Ross NE, Archer JA. Read length and repeat resolution: exploring prokaryote genomes using next-generation sequencing technologies. PLoS One 2010, 5:e11518. 10.1371/journal.pone.0011518, 2902515, 20634954.
39. Zhang T, Zhang X, Hu S, Jun Y. An efficient procedure for plant organellar genome assembly, based on whole genome data from the 454 GS FLX sequencing platform. Plant methods 2011, 7:38. 10.1186/1746-4811-7-38, 3248859, 22126655.
40. Nielsen CB, Jackman SD, Birol I, Jones SJ. ABySS-Explorer: visualizing genome sequence assemblies. IEEE Trans Vis Comput Graph 2009, 15:881-888.
41. Kircher M, Kelso J. High-throughput DNA sequencing concepts and limitations. Bioessays 2010, 32:524-536. 10.1002/bies.200900181, 20486139.
42. Aury JM, Cruaud C, Barbe V, Rogier O, Mangenot S, Samson G, Poulain J, Anthouard V, Scarpelli C, Artiguenave F, Wincker P. High quality draft sequences for prokaryotic genomes using a mix of new sequencing technologies. BMC Genomics 2008, 9:603. 10.1186/1471-2164-9-603, 2625371, 19087275.
43. Robison MM, Wolyn DJ. Complex organization of the mitochondrial genome of petaloid CMS carrot. Mol Genet Genomics 2002, 268:232-239. 10.1007/s00438-002-0740-z, 12395197.
44. Adams KL, Qiu YL, Stoutemyer M, Palmer JD. 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 2002, 99:9905-9912. 10.1073/pnas.042694899, 126597, 12119382.
45. Figueroa P, Gómez I, Holuigue L, Araya A, Jordana X. Transfer of rps14 from the mitochondrion to the nucleus in maize implied integration within a gene encoding the iron sulphur subunit of succinate dehydrogenase and expression by alternative splicing. Plant J 1999, 18:601-609. 10.1046/j.1365-313x.1999.00485.x, 10417711.
46. Adams KL, Daley DO, Qiu YL, Whelan J, Palmer JD. Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature 2000, 408:354-357. 10.1038/35042567, 11099041.
47. Adams KL, Rosenblueth M, Qiu Y, Palmer JD. Multiple losses and transfers to the nucleus of two mitochondrial succinate dehydrogenase genes during angiosperm evolution. Genetics 2001, 158:1289-1300. 1461739, 11454775.
48. Adams KL, Daley DO, Whelan J, Palmer JD. Genes for two mitochondrial ribosomal proteins in flowering plants are derived from their chloroplast or cytosolic counterparts. Plant Cell 2002, 14:931-943. 10.1105/tpc.010483, 150693, 11971146.
49. Liu S, Zhuang Y, Zhang P, Adams KL. Comparative analysis of structural diversity and sequence evolution in plant mitochondrial genes transferred to the nucleus. Mol Biol Evol 2009, 26:875-891. 10.1093/molbev/msp011, 19168566.
50. Kubo N, Arimura S. Discovery of the rpl10 gene in diverse plant mitochondrial genomes and its probable replacement by the nuclear gene for chloroplast RPL10 in two lineages of angiosperms. DNA Res 2010, 17:1-9. 10.1093/dnares/dsp024, 2818186, 19934175.
51. Knoop V, Volkmar U, Hecht J, Grewe F. Mitochondrial genome evolution in the plant lineage. Plant Mitochondria. Volume 1 2011, 3-29. Springer, New York, Kempken F.
52. Marechal A, Brisson N. Recombination and the maintenance of plant organelle genome stability. New Phytol 2010, 186:299-317. 10.1111/j.1469-8137.2010.03195.x, 20180912.
53. Alverson AJ, Rice DW, Dickinson S, Barry K, Palmer JD. Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 2011, 23:2499-2513. 10.1105/tpc.111.087189, 3226218, 21742987.
54. Sloan D, Alverson A, Storchova H, Palmer J, Taylor D. Extensive loss of translational genes in the structurally dynamic mitochondrial genome of the angiosperm Silene latifolia. BMC Evol Biol 2010, 10:274. 10.1186/1471-2148-10-274, 2942850, 20831793.
55. Woloszynska M, Trojanowski D. Counting mtDNA molecules in Phaseolus vulgaris: sublimons are constantly produced by recombination via short repeats and undergo rigorous selection during substoichiometric shifting. Plant Mol Biol 2009, 70:511-521. 10.1007/s11103-009-9488-8, 19387845.
56. Woloszynska M. Heteroplasmy and stoichiometric complexity of plant mitochondrial genomes though this be madness, yet there's method in't. J Exp Bot 2010, 61:657-671. 10.1093/jxb/erp361, 19995826.
57. Davila J, Arrieta-Montiel M, Wamboldt Y, Cao J, Hagmann J, Shedge V, Xu Y, Weigel D, Mackenzie S. Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 2011, 9:64. 10.1186/1741-7007-9-64, 3193812, 21951689.
58. Gray MW, Burger G, Lang BF. Mitochondrial Evolution. Science 1999, 283(5407):1476-1481. 10.1126/science.283.5407.1476, 10066161.
59. Timmis JN, Ayliffe MA, Huang CY, Martin W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 2004, 5:123-135.
60. Archibald JM. The puzzle of plastid evolution. Curr Biol 2009, 19:R81-R88. 10.1016/j.cub.2008.11.067, 19174147.
61. Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD. Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 1991, 10:3073-3078. 453023, 1915281.
62. Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L, Kavanagh TA, Hibberd JM, Gray JC, Morden CW, Calie PJ, Jermiin LS, Wolfe KH. Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell 2001, 13:645-658. 135507, 11251102.
63. Notsu YN, Masood SM, Nishikawa TN, Kubo NK, Akiduki GA, Nakazono MN, Hirai AH, Kadowaki KK. 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 2002, 268:434-445. 10.1007/s00438-002-0767-1, 12471441.
64. Downie SR, Katz-Downie DS, Spalik K. A phylogeny of Apiaceae tribe Scandiceae: evidence from nuclear ribosomal DNA internal transcribed spacer sequences. Am J Bot 2000, 87:76-95. 10.2307/2656687, 10636832.
65. Burger G, Gray MW, Franz Lang B. Mitochondrial genomes: anything goes. Trends Genet 2003, 19:709-716. 10.1016/j.tig.2003.10.012, 14642752.
66. Fan W, Woelfle MA, Mosig G. Two copies of a DNA element, " Wendy" , in the chloroplast chromosome of Chlamydomonas reinhardtii between rearranged gene clusters. Plant Mol Biol 1995, 29:63-80. 10.1007/BF00019119, 7579168.
67. Simon PW, Peterson PE. B493 and B9304, carrot inbreds for use in breeding, genetics, and tissue culture. Hortscience 1990, 25:815.
68. Murray MG, Thompson WF. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 1980, 8:4321-4326. 10.1093/nar/8.19.4321, 324241, 7433111.
69. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol 2004, 5(2):R12. 10.1186/gb-2004-5-2-r12, 395750, 14759262.
70. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 2005, 33:W686-W689. 10.1093/nar/gki366, 1160127, 15980563.