Massive Mitochondrial Gene Transfer in a Parasitic Flowering Plant Clade

PLoS Genetics

Volumn 9, Issue 2, 2013, Pages

  Xi, Zhenxiang ^a   Wang, Yuguo ^b,c   Bradley, Robert K ^d   Sugumaran, M ^e   Marx, Christopher J ^a,f   Rest, Joshua S ^g   Davis, Charles C ^a  

^a HARVARD UNIVERSITY   (United States)

^b FUDAN UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

^d Fred Hutchinson Cancer Research Center   (United States)

^e UNIVERSITY OF MALAYA   (Malaysia)

^f HARVARD UNIVERSITY   (United States)

^g STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOSPERM; ARTICLE; CLADISTICS; GENETIC TRANSCRIPTION; HOMOLOGOUS RECOMBINATION; HORIZONTAL GENE TRANSFER; MITOCHONDRIAL GENE; NONHUMAN; PARASITIC PLANT; PHYLOGENY; RAFFLESIA CANTLEYI; RNA SEQUENCE; SYNTENY; TRANSGENE;

DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FLOWERS; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; GENOME, PLANT; HOST-PARASITE INTERACTIONS; PHYLOGENY; PLANTS; RNA, RIBOSOMAL; SYMBIOSIS;

EID: 84874771840     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003265     Document Type: Article

References (63)

1. Richardson AO, Palmer JD, (2007) Horizontal gene transfer in plants. J Exp Bot 58: 1-9.
2. Bock R, (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15: 11-22.
3. Won H, Renner SS, (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100: 10824-10829.
4. Bergthorsson U, Adams KL, Thomason B, Palmer JD, (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197-201.
5. Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD, (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101: 17747-17752.
6. Sanchez-Puerta MV, Cho Y, Mower JP, Alverson AJ, Palmer JD, (2008) Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria. Mol Biol Evol 25: 1762-1777.
7. Mower JP, Stefanovic S, Hao W, Gummow JS, Jain K, et al. (2010) Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8: 150.
8. Davis CC, Wurdack KJ, (2004) Host-to-parasite gene transfer in flowering plants: Phylogenetic evidence from Malpighiales. Science 305: 676-678.
9. Mower JP, Stefanovic S, Young GJ, Palmer JD, (2004) Gene transfer from parasitic to host plants. Nature 432: 165-166.
10. Nickrent DL, Blarer A, Qiu YL, Vidal-Russell R, Anderson FE, (2004) Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol 4: 40.
11. Park JM, Manen JF, Schneeweiss GM, (2007) Horizontal gene transfer of a plastid gene in the non-photosynthetic flowering plants Orobanche and Phelipanche (Orobanchaceae). Mol Phylogenet Evol 43: 974-985.
12. Yoshida S, Maruyama S, Nozaki H, Shirasu K, (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328: 1128.
13. Barkman TJ, McNeal JR, Lim SH, Coat G, Croom HB, et al. (2007) Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 7: 248.
14. Stegemann S, Bock R, (2009) Exchange of genetic material between cells in plant tissue grafts. Science 324: 649-651.
15. Stegemann S, Keuthe M, Greiner S, Bock R, (2012) Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA 109: 2434-2438.
16. Barkman TJ, Lim SH, Salleh KM, Nais J, (2004) Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world's largest flower. Proc Natl Acad Sci USA 101: 787-792.
17. Davis CC, Latvis M, Nickrent DL, Wurdack KJ, Baum DA, (2007) Floral gigantism in Rafflesiaceae. Science 315: 1812.
18. Wurdack KJ, Davis CC, (2009) Malpighiales phylogenetics: gaining ground on one of the most recalcitrant clades in the angiosperm tree of life. Am J Bot 96: 1551-1570.
19. Chan AP, Crabtree J, Zhao Q, Lorenzi H, Orvis J, et al. (2010) Draft genome sequence of the oilseed species Ricinus communis. Nat Biotechnol 28: 951-956.
20. Rivarola M, Foster JT, Chan AP, Williams AL, Rice DW, et al. (2011) Castor bean organelle genome sequencing and worldwide genetic diversity analysis. PLoS ONE 6: e21743 doi:10.1371/journal.pone.0021743.
21. Jansen RK, Kaittanis C, Saski C, Lee SB, Tomkins J, et al. (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6: 32.
22. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
23. Goremykin VV, Salamini F, Velasco R, Viola R, (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26: 99-110.
24. Wikström N, Savolainen V, Chase MW, (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc B 268: 2211-2220.
25. Magallón S, Castillo A, (2009) Angiosperm diversification through time. Am J Bot 96: 349-365.
26. Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, et al. (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106: 3853-3858.
27. Bell CD, Soltis DE, Soltis PS, (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97: 1296-1303.
28. Xi Z, Bradley RK, Wurdack KJ, Wong KM, Sugumaran M, et al. (2012) Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics 13: 227.
29. Adams KL, Qiu YL, Stoutemyer M, Palmer JD, (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.
30. Jansen RK, Raubeson LA, Boore JL, DePamphilis CW, Chumley TW, et al. (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Method Enzymol 395: 348-384.
31. Nickrent DL, Yan OY, Duff RJ, dePamphilis CW, (1997) Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Mol Biol 34: 717-729.
32. Draper CK, Hays JB, (2000) Replication of chloroplast, mitochondrial and nuclear DNA during growth of unirradiated and UVB-irradiated Arabidopsis leaves. Plant J 23: 255-265.
33. Hiesel R, Wissinger B, Schuster W, Brennicke A, (1989) RNA editing in plant mitochondria. Science 246: 1632-1634.
34. Nais J (2001) Rafflesia of the world: Kota Kinabalu: Sabah Parks.
35. Veldkamp JF, (2008) The correct name for the Tetrastigma (Vitaceae) host of Rafflesia (Rafflesiaceae) in Malesia and a (not so) new species. Reinwardtia 12: 261-265.
36. Soejima A, Wen J, (2006) Phylogenetic analysis of the grape family (Vitaceae) based on three chloroplast markers. Am J Bot 93: 278-287.
37. Ren H, Lu LM, Soejima A, Luke Q, Zhang DX, et al. (2011) Phylogenetic analysis of the grape family (Vitaceae) based on the noncoding plastid trnC-petN, trnH-psbA, and trnL-F sequences. Taxon 60: 629-637.
38. Bremer B, Bremer K, Chase MW, Fay MF, Reveal JL, et al. (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161: 105-121.
39. Hillis DM, Bull JJ, (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42: 182-192.
40. Qiu Y-L, Li L, Wang B, Xue J-Y, Hendry TA, et al. (2010) Angiosperm phylogeny inferred from sequences of four mitochondrial genes. J Syst Evol 48: 391-425.
41. Thomas CM, Nielsen KM, (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Rev Microbiol 3: 711-721.
42. Hao W, Palmer JD, (2009) Fine-scale mergers of chloroplast and mitochondrial genes create functional, transcompartmentally chimeric mitochondrial genes. Proc Natl Acad Sci USA 106: 16728-16733.
43. Arimura S, Yamamoto J, Aida GP, Nakazono M, Tsutsumi N, (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci USA 101: 7805-7808.
44. Sheahan MB, McCurdy DW, Rose RJ, (2005) Mitochondria as a connected population: ensuring continuity of the mitochondrial genome during plant cell dedifferentiation through massive mitochondrial fusion. Plant J 44: 744-755.
45. Logan DC, (2010) Mitochondrial fusion, division and positioning in plants. Biochem Soc Trans 38: 789-795.
46. Woloszynska M, Bocer T, Mackiewicz P, Janska H, (2004) A fragment of chloroplast DNA was transferred horizontally, probably from non-eudicots, to mitochondrial genome of Phaseolus. Plant Mol Biol 56: 811-820.
47. Sanchez-Puerta MV, Abbona CC, Zhuo S, Tepe EJ, Bohs L, et al. (2011) Multiple recent horizontal transfers of the cox1 intron in Solanaceae and extended co-conversion of flanking exons. BMC Evol Biol 11: 277.
48. Bendiksby M, Schumacher T, Gussarova G, Nais J, Mat-Salleh K, et al. (2010) Elucidating the evolutionary history of the Southeast Asian, holoparasitic, giant-flowered Rafflesiaceae: Pliocene vicariance, morphological convergence and character displacement. Mol Phylogenet Evol 57: 620-633.
49. Chen PT, Wen J, Chen LQ, (2011) Spatial and temporal diversification of Tetrastigma Planch. (Vitaceae). Gard Bull Singapore 63: 313-333.
50. Davis CC, Anderson WR, Wurdack KJ, (2005) Gene transfer from a parasitic flowering plant to a fern. Proc R Soc B 272: 2237-2242.
51. Hao W, (2010) OrgConv: detection of gene conversion using consensus sequences and its application in plant mitochondrial and chloroplast homologs. BMC Bioinformatics 11: 114.
52. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
53. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, et al. (2009) ABySS: A parallel assembler for short read sequence data. Genome Res 19: 1117-1123.
54. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
55. Enright AJ, van Dongen S, Ouzounis CA, (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575-1584.
56. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
57. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
58. Kim D, Salzberg SL, (2011) TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 12: R72.
59. Stamatakis A, (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
60. Stamatakis A, Hoover P, Rougemont J, (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758-771.
61. Shimodaira H, (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51: 492-508.
62. Shimodaira H, (2008) Testing regions with nonsmooth boundaries via multiscale bootstrap. J Stat Plan Infer 138: 1227-1241.
63. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.