Massive Mitochondrial Gene Transfer in a Parasitic Flowering Plant Clade
Recent studies have suggested that plant genomes have undergone potentially rampant horizontal gene transfer (HGT), especially in the mitochondrial genome. Parasitic plants have provided the strongest evidence of HGT, which appears to be facilitated by the intimate physical association between the parasites and their hosts. A recent phylogenomic study demonstrated that in the holoparasite Rafflesia cantleyi (Rafflesiaceae), whose close relatives possess the world's largest flowers, about 2.1% of nuclear gene transcripts were likely acquired from its obligate host. Here, we used next-generation sequencing to obtain the 38 protein-coding and ribosomal RNA genes common to the mitochondrial genomes of angiosperms from R. cantleyi and five additional species, including two of its closest relatives and two host species. Strikingly, our phylogenetic analyses conservatively indicate that 24%–41% of these gene sequences show evidence of HGT in Rafflesiaceae, depending on the species. Most of these transgenic sequences possess intact reading frames and are actively transcribed, indicating that they are potentially functional. Additionally, some of these transgenes maintain synteny with their donor and recipient lineages, suggesting that native genes have likely been displaced via homologous recombination. Our study is the first to comprehensively assess the magnitude of HGT in plants involving a genome (i.e., mitochondria) and a species interaction (i.e., parasitism) where it has been hypothesized to be potentially rampant. Our results establish for the first time that, although the magnitude of HGT involving nuclear genes is appreciable in these parasitic plants, HGT involving mitochondrial genes is substantially higher. This may represent a more general pattern for other parasitic plant clades and perhaps more broadly for angiosperms.
Vyšlo v časopise:
Massive Mitochondrial Gene Transfer in a Parasitic Flowering Plant Clade. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003265
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003265
Souhrn
Recent studies have suggested that plant genomes have undergone potentially rampant horizontal gene transfer (HGT), especially in the mitochondrial genome. Parasitic plants have provided the strongest evidence of HGT, which appears to be facilitated by the intimate physical association between the parasites and their hosts. A recent phylogenomic study demonstrated that in the holoparasite Rafflesia cantleyi (Rafflesiaceae), whose close relatives possess the world's largest flowers, about 2.1% of nuclear gene transcripts were likely acquired from its obligate host. Here, we used next-generation sequencing to obtain the 38 protein-coding and ribosomal RNA genes common to the mitochondrial genomes of angiosperms from R. cantleyi and five additional species, including two of its closest relatives and two host species. Strikingly, our phylogenetic analyses conservatively indicate that 24%–41% of these gene sequences show evidence of HGT in Rafflesiaceae, depending on the species. Most of these transgenic sequences possess intact reading frames and are actively transcribed, indicating that they are potentially functional. Additionally, some of these transgenes maintain synteny with their donor and recipient lineages, suggesting that native genes have likely been displaced via homologous recombination. Our study is the first to comprehensively assess the magnitude of HGT in plants involving a genome (i.e., mitochondria) and a species interaction (i.e., parasitism) where it has been hypothesized to be potentially rampant. Our results establish for the first time that, although the magnitude of HGT involving nuclear genes is appreciable in these parasitic plants, HGT involving mitochondrial genes is substantially higher. This may represent a more general pattern for other parasitic plant clades and perhaps more broadly for angiosperms.
Zdroje
1. RichardsonAO, PalmerJD (2007) Horizontal gene transfer in plants. J Exp Bot 58: 1–9.
2. BockR (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15: 11–22.
3. WonH, RennerSS (2003) Horizontal gene transfer from flowering plants to Gnetum. Proc Natl Acad Sci USA 100: 10824–10829.
4. BergthorssonU, AdamsKL, ThomasonB, PalmerJD (2003) Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197–201.
5. BergthorssonU, RichardsonAO, YoungGJ, GoertzenLR, PalmerJD (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-PuertaMV, ChoY, MowerJP, AlversonAJ, PalmerJD (2008) Frequent, phylogenetically local horizontal transfer of the cox1 group I intron in flowering plant mitochondria. Mol Biol Evol 25: 1762–1777.
7. MowerJP, StefanovicS, HaoW, GummowJS, JainK, 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. DavisCC, WurdackKJ (2004) Host-to-parasite gene transfer in flowering plants: Phylogenetic evidence from Malpighiales. Science 305: 676–678.
9. MowerJP, StefanovicS, YoungGJ, PalmerJD (2004) Gene transfer from parasitic to host plants. Nature 432: 165–166.
10. NickrentDL, BlarerA, QiuYL, Vidal-RussellR, AndersonFE (2004) Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol 4: 40.
11. ParkJM, ManenJF, SchneeweissGM (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. YoshidaS, MaruyamaS, NozakiH, ShirasuK (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328: 1128.
13. BarkmanTJ, McNealJR, LimSH, CoatG, CroomHB, 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. StegemannS, BockR (2009) Exchange of genetic material between cells in plant tissue grafts. Science 324: 649–651.
15. StegemannS, KeutheM, GreinerS, BockR (2012) Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA 109: 2434–2438.
16. BarkmanTJ, LimSH, SallehKM, NaisJ (2004) Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world's largest flower. Proc Natl Acad Sci USA 101: 787–792.
17. DavisCC, LatvisM, NickrentDL, WurdackKJ, BaumDA (2007) Floral gigantism in Rafflesiaceae. Science 315: 1812.
18. WurdackKJ, DavisCC (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. ChanAP, CrabtreeJ, ZhaoQ, LorenziH, OrvisJ, et al. (2010) Draft genome sequence of the oilseed species Ricinus communis. Nat Biotechnol 28: 951–956.
20. RivarolaM, FosterJT, ChanAP, WilliamsAL, RiceDW, et al. (2011) Castor bean organelle genome sequencing and worldwide genetic diversity analysis. PLoS ONE 6: e21743 doi:10.1371/journal.pone.0021743.
21. JansenRK, KaittanisC, SaskiC, LeeSB, TomkinsJ, 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. JaillonO, AuryJM, NoelB, PolicritiA, ClepetC, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463–467.
23. GoremykinVV, SalaminiF, VelascoR, ViolaR (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26: 99–110.
24. WikströmN, SavolainenV, ChaseMW (2001) Evolution of the angiosperms: calibrating the family tree. Proc R Soc B 268: 2211–2220.
25. MagallónS, CastilloA (2009) Angiosperm diversification through time. Am J Bot 96: 349–365.
26. WangH, MooreMJ, SoltisPS, BellCD, BrockingtonSF, et al. (2009) Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106: 3853–3858.
27. BellCD, SoltisDE, SoltisPS (2010) The age and diversification of the angiosperms re-revisited. Am J Bot 97: 1296–1303.
28. XiZ, BradleyRK, WurdackKJ, WongKM, SugumaranM, et al. (2012) Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics 13: 227.
29. AdamsKL, QiuYL, StoutemyerM, PalmerJD (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. JansenRK, RaubesonLA, BooreJL, DePamphilisCW, ChumleyTW, et al. (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Method Enzymol 395: 348–384.
31. NickrentDL, YanOY, DuffRJ, dePamphilisCW (1997) Do nonasterid holoparasitic flowering plants have plastid genomes? Plant Mol Biol 34: 717–729.
32. DraperCK, HaysJB (2000) Replication of chloroplast, mitochondrial and nuclear DNA during growth of unirradiated and UVB-irradiated Arabidopsis leaves. Plant J 23: 255–265.
33. HieselR, WissingerB, SchusterW, BrennickeA (1989) RNA editing in plant mitochondria. Science 246: 1632–1634.
34. Nais J (2001) Rafflesia of the world: Kota Kinabalu: Sabah Parks.
35. VeldkampJF (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. SoejimaA, WenJ (2006) Phylogenetic analysis of the grape family (Vitaceae) based on three chloroplast markers. Am J Bot 93: 278–287.
37. RenH, LuLM, SoejimaA, LukeQ, ZhangDX, 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. BremerB, BremerK, ChaseMW, FayMF, RevealJL, 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. HillisDM, BullJJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42: 182–192.
40. QiuY-L, LiL, WangB, XueJ-Y, HendryTA, et al. (2010) Angiosperm phylogeny inferred from sequences of four mitochondrial genes. J Syst Evol 48: 391–425.
41. ThomasCM, NielsenKM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Rev Microbiol 3: 711–721.
42. HaoW, PalmerJD (2009) Fine-scale mergers of chloroplast and mitochondrial genes create functional, transcompartmentally chimeric mitochondrial genes. Proc Natl Acad Sci USA 106: 16728–16733.
43. ArimuraS, YamamotoJ, AidaGP, NakazonoM, TsutsumiN (2004) Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc Natl Acad Sci USA 101: 7805–7808.
44. SheahanMB, McCurdyDW, RoseRJ (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. LoganDC (2010) Mitochondrial fusion, division and positioning in plants. Biochem Soc Trans 38: 789–795.
46. WoloszynskaM, BocerT, MackiewiczP, JanskaH (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-PuertaMV, AbbonaCC, ZhuoS, TepeEJ, BohsL, 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. BendiksbyM, SchumacherT, GussarovaG, NaisJ, Mat-SallehK, 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. ChenPT, WenJ, ChenLQ (2011) Spatial and temporal diversification of Tetrastigma Planch. (Vitaceae). Gard Bull Singapore 63: 313–333.
50. DavisCC, AndersonWR, WurdackKJ (2005) Gene transfer from a parasitic flowering plant to a fern. Proc R Soc B 272: 2237–2242.
51. HaoW (2010) OrgConv: detection of gene conversion using consensus sequences and its application in plant mitochondrial and chloroplast homologs. BMC Bioinformatics 11: 114.
52. BentleyDR, BalasubramanianS, SwerdlowHP, SmithGP, MiltonJ, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53–59.
53. SimpsonJT, WongK, JackmanSD, ScheinJE, JonesSJM, et al. (2009) ABySS: A parallel assembler for short read sequence data. Genome Res 19: 1117–1123.
54. AltschulSF, MaddenTL, SchafferAA, ZhangJH, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
55. EnrightAJ, van DongenS, OuzounisCA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575–1584.
56. KatohK, MisawaK, KumaK, MiyataT (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059–3066.
57. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
58. KimD, SalzbergSL (2011) TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 12: R72.
59. StamatakisA (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
60. StamatakisA, HooverP, RougemontJ (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57: 758–771.
61. ShimodairaH (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51: 492–508.
62. ShimodairaH (2008) Testing regions with nonsmooth boundaries via multiscale bootstrap. J Stat Plan Infer 138: 1227–1241.
63. MortazaviA, WilliamsBA, McCueK, SchaefferL, WoldB (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621–628.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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