A Functional Phylogenomic View of the Seed Plants

English version České info

A novel result of the current research is the development and implementation of a unique functional phylogenomic approach that explores the genomic origins of seed plant diversification. We first use 22,833 sets of orthologs from the nuclear genomes of 101 genera across land plants to reconstruct their phylogenetic relationships. One of the more salient results is the resolution of some enigmatic relationships in seed plant phylogeny, such as the placement of Gnetales as sister to the rest of the gymnosperms. In using this novel phylogenomic approach, we were also able to identify overrepresented functional gene ontology categories in genes that provide positive branch support for major nodes prompting new hypotheses for genes associated with the diversification of angiosperms. For example, RNA interference (RNAi) has played a significant role in the divergence of monocots from other angiosperms, which has experimental support in Arabidopsis and rice. This analysis also implied that the second largest subunit of RNA polymerase IV and V (NRPD2) played a prominent role in the divergence of gymnosperms. This hypothesis is supported by the lack of 24nt siRNA in conifers, the maternal control of small RNA in the seeds of flowering plants, and the emergence of double fertilization in angiosperms. Our approach takes advantage of genomic data to define orthologs, reconstruct relationships, and narrow down candidate genes involved in plant evolution within a phylogenomic view of species' diversification.

Vyšlo v časopise: A Functional Phylogenomic View of the Seed Plants. PLoS Genet 7(12): e32767. doi:10.1371/journal.pgen.1002411
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002411

Souhrn

Zdroje

1. BurleighJGMathewsS 2004 Phylogenetic signal in nucleotide data from seed plants: implications for resolving the seed plant tree of life. Am J Bot 91 1599 1613

2. MathewsS 2009 Phylogenetic relationships among seed plants: persistent questions and the limits of molecular data. Am J Bot 96 228 236

3. BarkmanTJMcNealJRLimSHCoatGCroomHB 2007 Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol Biol 7 248

4. Bouchenak-KhelladiYSalaminNSavolainenVForestFBankM 2008 Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47 488 505

5. BoweLMCoatGdePamphilisCW 2000 Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proc Natl Acad Sci U S A 97 4092 4097

6. BurleighJGHiluKWSoltisDE 2009 Inferring phylogenies with incomplete data sets: a 5-gene, 567-taxon analysis of angiosperms. BMC Evol Biol 9 61

7. ChaseMWSoltisDEOlmsteadRGMorganDLesDH 1993 Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Missouri Bot Gard 80 528 580

8. SmithSADonoghueMJ 2008 Rates of molecular evolution are linked to life history in flowering plants. Science 322 86 89

9. ZhuXYChaseMWQiuYLKongHZDilcherDL 2007 Mitochondrial matR sequences help to resolve deep phylogenetic relationships in rosids. BMC Evol Biol 7 217

10. Leebens-MackJRaubesonLACuiLKuehlJVFourcadeMH 2005 Identifying the basal angiosperm node in chloroplast genome phylogenies: sampling one's way out of the Felsenstein zone. Mol Biol Evol 22 1948 1963

11. BraukmannTWKuzminaMStefanovicS 2009 Loss of all plastid ndh genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr Genet 55 323 337

12. JansenRKCaiZRaubesonLADaniellHDepamphilisCW 2007 Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A 104 19369 19374

13. McCoySRKuehlJVBooreJLRaubesonLA 2008 The complete plastid genome sequence of Welwitschia mirabilis: an unusually compact plastome with accelerated divergence rates. BMC Evol Biol 8 130

14. MooreMJBellCDSoltisPSSoltisDE 2007 Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A 104 19363 19368

15. QiuYLLiLWangBChenZKnoopV 2006 The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci U S A 103 15511 15516

16. ZhongBYonezawaTZhongYHasegawaM 2010 The position of Gnetales among seed plants: overcoming pitfalls of chloroplast phylogenomics. Mol Biol Evol 27 2855 2863

17. BurleighJGBansalMSEulensteinOHartmannSWeheA 2011 Genome-scale phylogenetics: inferring the plant tree of life from 18,896 gene trees. Syst Biol 60 117 125

18. FinetCTimmeREDelwicheCFMarlétazF 2010 Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20 2217 2222

19. SandersonMMcMahonM 2007 Inferring angiosperm phylogeny from EST data with widespread gene duplication. BMC Evol Biol 7 S3

20. BakerRHDeSalleR 1997 Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Syst Biol 46 654 673

21. ChiuJCLeeEKEganMGSarkarINCoruzziGM 2006 OrthologID: automation of genome-scale ortholog identification within a parsimony framework. Bioinformatics 22 699 707

22. KatariMSNowickiSDAceitunoFFNeroDKelferJ 2010 VirtualPlant: a software platform to support systems biology research. Plant Physiol 152 500 515

23. SchmidtMSchneider-PoetschHA 2002 The evolution of gymnosperms redrawn by phytochrome genes: the Gnetatae appear at the base of the gymnosperms. J Mol Evol 54 715 724

24. NixonKCCrepetWLStevensonDFriisEM 1994 A reevaluation of seed plant phylogeny. Ann Missouri Bot Gard 81 484 533

25. RothwellGWSerbetR 1994 Lignophyte phylogeny and the evolution of spermatophytes: a numerical cladistic analysis. Syst Bot 19 443 482

26. AlbertVABacklundABremerKChaseMWManhartJR 1994 Functional constraints and rbcL evidence for land plant phylogeny. Ann Missouri Bot Gard 81 534 567

27. GoremykinVBobrovaVPahnkeJTroitskyAAntonovA 1996 Noncoding sequences from the slowly evolving chloroplast inverted repeat in addition to rbcL data do not support gnetalean affinities of angiosperms. Mol Biol Evol 13 383 396

28. HasebeMKofujiRItoMKatoMIwatsukiK 1992 Phylogeny of gymnosperms inferred from rbcL gene sequences. J Plant Res 105 673 679

29. SamigullinTKMartinWFTroitskyAVAntonovAS 1999 Molecular data from the chloroplast rpoC1 gene suggest a deep and distinct dichotomy of contemporary spermatophytes into two monophyla: gymnosperms (including Gnetales) and angiosperms. J Mol Evol 49 310 315

30. MathewsSDonoghueMJ. Analyses of phytochrome data from seed plants: exploration of conflicting results from parsimony and Bayesian approaches; 2002 Aug 2-7; Madison, WI

31. BeckerATheissenG 2003 The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29 464 489

32. WinterKUBeckerAMunsterTKimJTSaedlerH 1999 MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc Natl Acad Sci U S A 96 7342 7347

33. FrohlichMWParkerDS 2000 The mostly male theory of flower evolutionary origins: from genes to fossils. Syst Bot 25 155 170

34. PearsonPN 1999 Apomorphy distribution is an important aspect of cladogram symmetry. Syst Biol 48 399 406

35. The Angiosperm Phylogeny Group 2003 An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141 399 436

36. The Angiosperm Phylogeny Group 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

37. WikstromNSavolainenVChaseMW 2001 Evolution of the angiosperms: calibrating the family tree. Proc R Soc B Biol Sci 268 2211 2220

38. ChaseMWFayMFDeveyDSRønstedNDaviesJ 2006 Multi-gene analyses of monocot relationships: a summary. Aliso 22 63 76

39. ChaseMWSoltisDESoltisPSRudallPJFayMF 2000 Higher-level systematics of the monocotyledons: an assessment of current knowledge and a new classification. WilsonKLMorrisonDA Monocots: Systematics and Evolution Melbourne CSIRO 1 16

40. ChaseMWStevensonDWWilkinPRudallPJ 1995 Monocot systematics: a combined analysis. RudallPJCribbPJCutlerDFHumphriesCJ Monocotyledons: Systematics and Evolution: Royal Botanical Gardens, Kew 685 730

41. DuvallMRLearnGHJrEguiarteLECleggMT 1993 Phylogenetic analysis of rbcL sequences identifies Acorus calamus as the primal extant monocotyledon. Proc Natl Acad Sci U S A 90 4641 4644

42. DavisJIPetersenGSebergOStevensonDWHardyCR 2006 Are mitochondrial genes useful for the analysis of monocot relationships? Taxon 55 857 870

43. DavisJIStevensonDWPetersenGSebergOCampbellLM 2004 A phylogeny of the monocots, as inferred from rbcL and atpA sequence variation, and a comparison of methods for calculating jackknife and bootstrap values. Syst Bot 29 467 510

44. StevensonDDavisJFreudensteinJVHardyCRSimmonsMP 2000 A phylogenetic analysis of the monocotyledons based on morphological and molecular character sets, with comments on the placement of Acorus and Hydatellaceae. WilsonKLMorrisonDA Monocots: Systematics and Evolution Melbourne CSIRO 17 24

45. SoltisDESoltisPSChaseMWMortMEAlbachDC 2000 Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 133 381 461

46. SoltisPSSoltisDEZanisMJKimS 2000 Basal lineages of angiosperms: relationships and implications for floral evolution. Intl J Plant Sci 161 S97 S107

47. ZanisMJSoltisDESoltisPSMathewsSDonoghueMJ 2002 The root of the angiosperms revisited. Proc Natl Acad Sci U S A 99 6848 6853

48. AshburnerMBallCABlakeJABotsteinDButlerH 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25 25 29

49. RosenfeldJADeSalleRLeeEKO'GradyP 2008 Using whole genome presence/absence data to untangle function in 12 Drosophila genomes. Fly 2 291 299

50. NielsenR 2005 Statistical Methods in Molecular Evolution. New York Springer 504

51. BiswasSAkeyJM 2006 Genomic insights into positive selection. Trends Genet 22 437 446

52. YangZBielawskiJP 2000 Statistical methods for detecting molecular adaptation. Trends Ecol Evol 15 496 503

53. MewesHWDietmannSFrishmanDGregoryRMannhauptG 2008 MIPS: analysis and annotation of genome information in 2007. Nucleic Acids Res 36 D196 201

54. Ohkama-OhtsuNZhaoPXiangCOliverDJ 2007 Glutathione conjugates in the vacuole are degraded by γ-glutamyl transpeptidase GGT3 in Arabidopsis. Plant J 49 878 888

55. RébeilléFJabrinSBlignyRLoizeauKGambonnetB 2006 Methionine catabolism in Arabidopsis cells is initiated by a γ-cleavage process and leads to S-methylcysteine and isoleucine syntheses. Proc Natl Acad Sci U S A 103 15687 15692

56. RizhskyLLiangHShumanJShulaevVDavletovaS 2004 When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134 1683 1696

57. CervillaLMBlascoBRiosJJRomeroLRuizJM 2007 Oxidative stress and antioxidants in tomato (Solanum lycopersicum) plants subjected to boron toxicity. Ann Bot 100 747 756

58. MateosRMLeonAMSandalioLMGomezMdel RioLA 2003 Peroxisomes from pepper fruits (Capsicum annuum L.): purification, characterisation and antioxidant activity. J Plant Physiol 160 1507 1516

59. AndersonJVDavisDG 2004 Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula. Physiol Plantarum 120 421 433

60. BhatiaKRahmanSAliMRaisuddinS 2006 In vitro antioxidant activity of Juglans regia L. bark extract and its protective effect on cyclophosphamide-induced urotoxicity in mice. Redox Rep 11 273 279

61. Rodriguez MillaMAMaurerARodriguez HueteAGustafsonJP 2003 Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. Plant J 36 602 615

62. Gross-HardtRKagiCBaumannNMooreJMBaskarR 2007 LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5 e47 doi:10.1371/journal.pbio.0050047

63. KidnerCAMartienssenRA 2004 Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428 81 84

64. Hernandez-PinzonIYelinaNESchwachFStudholmeDJBaulcombeD 2007 SDE5, the putative homologue of a human mRNA export factor, is required for transgene silencing and accumulation of trans-acting endogenous siRNA. Plant J 50 140 148

65. Cibrián-JaramilloADe la Torre-BarcenaJELeeEKKatariMSLittleDP 2010 Using phylogenomic patterns and gene ontology to identify proteins of importance in plant evolution. Genome Biol Evol 2 225 239

66. NagasakiHItohJHayashiKHibaraKSatoh-NagasawaN 2007 The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci U S A 104 14867 14871

67. MartienssenR 2010 Molecular biology. Small RNA makes its move. Science 328 834 835

68. MorinRDAksayGDolgosheinaEEbhardtHAMagriniV 2008 Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res 18 571 584

69. AxtellMJSnyderJABartelDP 2007 Common functions for diverse small RNAs of land plants. Plant Cell 19 1750 1769

70. RabinowiczPDCitekRBudimanMANunbergABedellJA 2005 Differential methylation of genes and repeats in land plants. Genome Res 15 1431 1440

71. MosherRAMelnykCWKellyKADunnRMStudholmeDJ 2009 Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460 283 286

72. Olmedo-MonfilVDuran-FigueroaNArteaga-VazquezMDemesa-ArevaloEAutranD 2010 Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464 628 632

73. FriedmanWE 2009 The meaning of Darwin's ‘abominable mystery’. Am J Bot 96 5 21

74. WeedallGDPolleySDConwayDJ 2008 Gene-specific signatures of elevated non-synonymous substitution rates correlate poorly across the Plasmodium genus. PLoS ONE 3 e2281 doi:10.1371/journal.pone.0002281

75. MagallónSASandersonMJSoltisP 2005 Angiosperm divergence times: the effect of genes, codon positions, and time constraints. Evolution 59 1653 1670

76. GovaertsRFrodinDGRadcliffe-SmithA 2000 World checklist and bibliography of Euphorbiaceae (with Pandaceae). 4 Volumes. London Royal Botanic Gardens, Kew

77. Radcliffe-SmithA 2001 Genera Euphorbiacearum. London Royal Botanic Gardens, Kew 464

78. DavisCCWebbCOWurdackKJJaramilloCADonoghueMJ 2005 Explosive radiation of Malpighiales supports a mid-Cretaceous origin of modern tropical rain forests. Am Nat 165 E36 E65

79. WurdackKJHoffmannPChaseMW 2005 Molecular phylogenetic analysis of uniovulate Euphorbiaceae (Euphorbiaceae sensu stricto) using plastid rbcL and trnL-F DNA sequences. Am J Bot 92 1397 1420

80. ChristinP-AOsborneCPSageRFArakakiMEdwardsEJ 2011 C4 eudicots are not younger than C4 monocots. J Exp Bot 62 3171 3181

81. GoldmanNYangZ 1994 A codon-based model of nucleotide substitution for protein-coding DNA sequence. Mol Biol Evol 11 725 736

82. KatohKTohH 2008 Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9 286 298

83. SwoffordDL 2003 PAUP*: Phylogenetic Analysis Using Parsimony (and other methods). Sunderland, , MA Sinauer Associates

84. GoloboffPAFarrisJSNixonKC 2008 TNT, a free program for phylogenetic analysis. Cladistics 24 774 786

85. GoloboffPA 1999 Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15 415 428

86. NixonKC 1999 The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15 407 414

87. GatesyJO'GradyPBakerRH 1999 Corroboration among data sets in simultaneous analysis: hidden support for phylogenetic relationships among higher level artiodactyl taxa. Cladistics 15 271 313

88. SorensonMDFranzosaEA 2007 TreeRot. 3 ed. Boston Boston University

89. StamatakisAOttM 2008 Efficient computation of the phylogenetic likelihood function on multi-gene alignments and multi-core architectures. Phil Trans R Soc B Biol Sci 363 3977 3984

90. OttMZolaJStamatakisAAluruS 2007 Large-scale maximum likelihood-based phylogenetic analysis on the IBM BlueGene/L. Proceedings of the 2007 ACM/IEEE Conference on Supercomputing Reno, , NV ACM

91. StamatakisAOttM 2008 Exploiting fine-grained parallelism in the phylogenetic likelihood function with MPI, Pthreads, and OpenMP: a performance study. Pattern Recognition in Bioinformatics Berlin Springer 424 435

92. StamatakisA 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 2688 2690

93. JonesDTTaylorWRThorntonJM 1992 The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8 275 282

94. LanaveCPreparataGSacconeCSerioG 1984 A new method for calculating evolutionary substitution rates. J Mol Evol 20 86 93

95. StamatakisA 2006 Phylogenetic models of rate heterogeneity: a high performance computing perspective. IEEE International Parallel and Distributed Processing Symposium. Rhodes, Greece

96. YangZ 1994 Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. J Mol Evol 39 306 314

97. StamatakisAHooverPRougemontJ 2008 A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57 758 771

98. PattengaleNDAlipourMBininda-EmondsORPMoretBMEStamatakisA 2010 How many bootstrap replicates are necessary? J Comput Biol 17 337 354

99. AshburnerMBallCABlakeJABotsteinDButlerH 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25 25 29

100. MewesHWDietmannSFrishmanDGregoryRMannhauptG 2008 MIPS: analysis and annotation of genome information in 2007. Nucl Acids Res 36 D196 201

101. WangRTischnerRGutierrezRAHoffmanMXingX 2004 Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol 136 2512 2522

102. YangZ 2006 Computational Molecular Evolution. Oxford Oxford University Press 357

103. SharpPM 1997 In search of molecular darwinism. Nature 385 111 112

104. GoldingGBDeanAM 1998 The structural basis of molecular adaptation. Mol Biol Evol 15 355 369

105. YangZ 1998 Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15 568 573

106. YangZNielsenRGoldmanNPedersenAM 2000 Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155 431 449

107. Kosakovsky PondSLFrostSDWMuseSV 2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679

108. MuseSVGautBS 1994 A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol 11 715 724

109. HasegawaMKishinoHYanoT 1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22 160 174

110. Kosakovsky PondSLFrostSDW 2005 Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22 1208 1222