A precise chloroplast genome of Nelumbo nucifera (Nelumbonaceae) evaluated with Sanger, Illumina MiSeq, and PacBio RS II sequencing platforms: Insight into the plastid evolution of basal eudicots

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Wu, Zhihua ^a   Gui, Songtao ^a   Quan, Zhiwu ^b   Pan, Lei ^c   Wang, Shuzhen ^d   Ke, Weidong ^e   Liang, Dequan ^f   Ding, Yi ^a  

^a WUHAN UNIVERSITY   (China)

^b BGI SHENZHEN   (China)

^c JIANGHAN UNIVERSITY   (China)

^d HUANGGANG NORMAL UNIVERSITY   (China)

^e Wuhan National Field Observation and Research Station for Aquatic Vegetables   (China)

^f Nextomics Biosciences Co Ltd   (China)

Author keywords

Basal eudicots; Chloroplast genome sequencing; Divergence time; N. nucifera; PacBio RS II; Systematic position

Indexed keywords

CODON; RIBOSOME RNA; TRANSFER RNA;

CHLOROPLAST; CHLOROPLAST GENOME; CODON; DEVICES; DNA SEQUENCE; EVALUATION STUDY; GENETICS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NELUMBO; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASTID; PROCEDURES;

BASE SEQUENCE; CHLOROPLASTS; CODON; EVOLUTION, MOLECULAR; GENOME, CHLOROPLAST; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; NELUMBO; PHYLOGENY; PLASTIDS; RNA, RIBOSOMAL; RNA, TRANSFER; SEQUENCE ANALYSIS, DNA;

EID: 84988706092     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-014-0289-0     Document Type: Article

References (85)

1. Liu J, Qi ZC, Zhao YP, Fu CX, Jenny Xiang QY: Complete cpDNA genome sequence of Smilax china and phylogenetic placement of Liliales-influences of gene partitions and taxon sampling. Mol Phylogenet Evol 2012, 64(3):545-562.
2. Sodmergen ZQ: Why does biparental plastid inheritance revive in angiosperms? J Plant Res 2010, 123(2):201-206.
3. Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J, Muller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL: 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 2007, 104(49):19369-19374.
4. Moore MJ, Bell CD, Soltis PS, Soltis DE: Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A 2007, 104(49):19363-19368.
5. Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE: Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci U S A 2010, 107(10):4623-4628.
6. Olmstead R, Palmer JD: Chloroplast DNA systematics: a review of methods and data analysis. Am J Bot 1994, 81(9):1205-1224.
7. Li R, Ma PF, Wen J, Yi TS: Complete sequencing of five araliaceae chloroplast genomes and the phylogenetic implications. PLoS One 2013, 8(10):e78568.
8. Lin CP, Wu CS, Huang YY, Chaw SM: The complete chloroplast genome of Ginkgo biloba reveals the mechanism of inverted repeat contraction. Genome Biol Evol 2012, 4(3):374-381.
9. Martin G, Baurens FC, Cardi C, Aury JM, D'Hont A: The complete chloroplast genome of banana (Musa acuminata, Zingiberales): insight into plastid monocotyledon evolution. PLoS One 2013, 8(6):e67350.
10. Straub SC, Cronn RC, Edwards C, Fishbein M, Liston A: Horizontal transfer of DNA from the mitochondrial to the plastid genome and its subsequent evolution in milkweeds (apocynaceae). Genome Biol Evol 2013, 5(10):1872-1885.
11. Yang JB, Yang SX, Li HT, Yang J, Li DZ: Comparative chloroplast genomes of camellia species. PLoS One 2013, 8(8):e73053.
12. Yi X, Gao L, Wang B, Su YJ, Wang T: The complete chloroplast genome sequence of Cephalotaxus oliveri (Cephalotaxaceae): evolutionary comparison of cephalotaxus chloroplast DNAs and insights into the loss of inverted repeat copies in gymnosperms. Genome Biol Evol 2013, 5(4):688-698.
13. Crane PR, Herendeen PS: Cretaceous floras containing angiosperm flowers and fruits from eastern North America. Rev Palaeobot Palyno 1996, 90:321-340.
14. Upchurch GR, Crane PR, Drinnan AN: The megaflora from the Quantico locality (Upper Albian), lower cretaceous Potomac group of Virginia. Mem Virginia Mus Nat Hist 1994, 4:1-57.
15. Borsch T, Barthlott W: Classification and distribution of the genus Nelumbo Adans. (Nelumbonaceae). Beitr Biol Pfl 1994, 68:421-450.
16. Cronquist A: An Integrated System of Classification of Flowering Plants. New York: Columbia University Press; 1981.
17. Ito M: Phylogenetic systematics of the Nymphaeales. Bot Mag Tokyo 1987, 100:17-35.
18. Les D: The origin and affinities of the Ceratophyllaceae. Taxon 1988, 37:326-345.
19. Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu YL, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Sysma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedren M, Gaut BS, Jansen RK, Kim KJ, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang QY, Plunkett GM, et al: Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Ann Missouri Bot Gard 1993, 80:528-580.
20. Hilu K, Borsch T, Muller K, Soltis DE, Pea S: Inference of angiosperm phylogeny based on matK sequence information. Am J Bot 2003, 90:1758-1776.
21. Hoot SB, Magallon S, Crane PR: Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18 s nuclear ribosomal DNA sequences. Ann Missouri Bot Gard 1999, 86:1-32.
22. Kim KJ, Lee HL: Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res 2004, 11(4):247-261.
23. Savolainen V, Chase MW, Hoot SB, Morton CM, Soltis DE, Bayer C, Fay MF, de Bruijn AY, Sullivan S, Qiu YL: Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences. Syst Biol 2000, 49:306-362.
24. Soltis DE, Soltis PS, Chase MW, Mort ME, Albach DC, Zanis M, Savolainen V, Hahn WH, Hoot SB, Fay MF: Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. Bot J Linn Soc 2000, 133:381-461.
25. Worberg A, Quandt D, Barniske A-M, Löhne C, Hilu KW, Borsch T: Phylogeny of basal eudicots: Insights from non-coding and rapidly evolving DNA. Org Divers Evol 2007, 7(1):55-77.
26. Wang Y, Fan GY, Liu YM, Sun FM, Shi CC, Liu X, Peng J, Chen WB, Huang XF, Cheng SF, Liu YP, Liang XM, Zhu HL, Bian C, Zhong L, Lv T, Dong HX, Liu WQ, Zhong X, Chen J, Quan ZW, Wang ZH, Tan BZ, Lin CF, Mu F, Xu X, Ding Y, Guo AY, Wang J, Ke WD: The sacred lotus genome provides insights into the evolution of flowering plants. Plant J 2013, 76(4):557-567.
27. Goremykin VV, Hirsch-Ernst KI, Wolfl S, Hellwig FH: Analysis of the Amborella trichopoda chloroplast genome sequence suggests that amborella is not a basal angiosperm. Mol Biol Evol 2003, 20(9):1499-1505.
28. Goremykin VV, Hirsch-Ernst KI, Wolfl S, Hellwig FH: The chloroplast genome of Nymphaea alba: whole-genome analyses and the problem of identifying the most basal angiosperm. Mol Biol Evol 2004, 21(7):1445-1454.
29. Kunnimalaiyaan M, Nielsen BL: Fine mapping of replication origins (oriA and oriB) in Nicotiana tabacum chloroplast DNA. Nucleic Acids Res 1997, 25:3681-3686.
30. Raubeson LA, Peery R, Chumley TW, Dziubek C, Fourcade HM, Boore JL, Jansen RK: Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics 2007, 8:174.
31. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S: Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 1999, 6:283-290.
32. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J, Heiner C, Clum A, Copeland A, Huddleston J, Eichler EE, Turner SW, Korlach J: Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013, 10(6):563-569.
33. Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y: A tale of three next generation sequencing platforms: comparison of Ion Torrent. Pacific Biosciences and Illumina MiSeq sequencers. BMC Genomics 2012, 13:341.
34. Roberts RJ, Carneiro MO, Schatz MC: The advantages of SMRT sequencing. Genome Biol 2013, 14(6):405.
35. Koren S, Schatz MC, Walenz BP, Martin J, Howard JT, Ganapathy G, Wang Z, Rasko DA, McCombie WR, Jarvis ED, Phillippy AM: Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat Biotechnol 2012, 30(7):693-700.
36. Loomis EW, Eid JS, Peluso P, Yin J, Hickey L, Rank D, McCalmon S, Hagerman RJ, Tassone F, Hagerman PJ: Sequencing the unsequenceable: expanded CGG-repeat alleles of the fragile X gene. Genome Res 2013, 23(1):121-128.
37. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, Greulich H, Lawrence MS, Lennon NJ, McKenna A, Meldrim J, Ramos AH, Ross MG, Russ C, Shefler E, Sivachenko A, Sogoloff B, Stojanov P, Tamayo P, Mesirov JP, Amani V, Teider N, Sengupta S, Francois JP, Northcott PA, Taylor MD, et al: Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 2012, 488(7409):106-110.
38. Fichot EB, Norman RS: Microbial phylogenetic profiling with the Pacific Biosciences sequencing platform. Microbiome 2013, 1(1):10.
39. Koren S, Harhay GP, Smith TP, Bono JL, Harhay DM, McVey SD, Radune D, Bergman NH, Phillippy AM: Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biol 2013, 14(9):R101.
40. Ferrarini M, Moretto M, Ward JA, Surbanovski N, Stevanovic V, Giongo L, Viola R, Cavalieri D, Velasco R, Cestaro A, Sargent DJ: An evaluation of the PacBio RS platform for sequencing and de novo assembly of a chloroplast genome. BMC Genomics 2013, 14:670.
41. Metzker ML: Sequencing technologies-the next generation. Nat Rev Genet 2010, 11(1):31-46.
42. Ricker N, Qian H, Fulthorpe RR: The limitations of draft assemblies for understanding prokaryotic adaptation and evolution. Genomics 2012, 100(3):167-175.
43. Moore MJ, Dhingra A, Soltis PS, Shaw R, Farmerie WG, Folta KM, Soltis DE: Rapid and accurate pyrosequencing of angiosperm plastid genomes. BMC Plant Biol 2006, 6:17.
44. 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.
45. Dong W, Xu C, Cheng T, Lin K, Zhou S: Sequencing angiosperm plastid genomes made easy: a complete set of universal primers and a case study on the phylogeny of Saxifragales. Genome Biol Evol 2013, 5(5):989-997.
46. Hirose T, Sugiura M: Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: a possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. EMBO J 1997, 16(22):6804-6811.
47. Tsudzuki T, Wakasugi T, Sugiura M: Comparative analysis of RNA editing sites in higher plant chloroplasts. J Mol Evol 2001, 53:327-332.
48. Sawai S, Thomason PA, Cox EC: An autoregulatory circuit for long-range self-organization in Dictyostelium cell populations. Nature 2005, 433(7023):323-326.
49. Kato T, Kaneko T, Sato S, Nakamura Y, Tabata S: Complete structure of the chloroplast genome of a legume, Lotus japonicus. DNA Res 2000, 7:323-330.
50. Wicke S, Muller KF, de Pamphilis CW, Quandt D, Wickett NJ, Zhang Y, Renner SS, Schneeweiss GM: Mechanisms of functional and physical genome reduction in photosynthetic and nonphotosynthetic parasitic plants of the broomrape family. Plant Cell 2013, 25(10):3711-3725.
51. Funk HT, Berg S, Krupinska K, Maier UG, Krause K: Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol 2007, 7:45.
52. de Pamphilis CW, Palmer JD: Loss of photosynthetic and chlororespiratory genes from the plastid genome of a parasitic flowering plant. Nature 1990, 348(6299):337-339.
53. Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH, Cheng CH, Lin CY, Liu SM, Chang CC, Chaw SM: The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol 2006, 23(2):279-291.
54. Weng ML, Blazier JC, Govindu M, Jansen RK: Reconstruction of the ancestral plastid genome in geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Mol Biol Evol 2014, 31(3):645-659.
55. Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M: Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci U S A 1994, 91(21):9794-9798.
56. 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(3):645-658.
57. Delannoy E, Fujii S, Des Francs-Small CC, Brundrett M, Small I: Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol 2011, 28(7):2077-2086.
58. Barth D, Berendonk TU: The mitochondrial genome sequence of the ciliate Paramecium caudatum reveals a shift in nucleotide composition and codon usage within the genus Paramecium. BMC Genomics 2011, 12:272.
59. Angiosperm Phylogeny Group: An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 2009, 161:105-121.
60. Kreunen SS, Osborn JM: Pollen and anther development in Nelumbo (Nelumbonaceae). Am J Bot 1999, 86(12):1662-1676.
61. Drinnan AN, Crane PR, Hoot SB: Patterns of floral evolution in the early diversification of non-magnoliid dicotyledons (eudicots). Plant Syst Evol 1994, 8:93-122.
62. Soltis PS, Soltis DE, Chase MW: Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 1999, 402:402-404.
63. Hansen DR, Dastidar SG, Cai Z, Penaflor C, Kuehl JV, Boore JL, Jansen RK: Phylogenetic and evolutionary implications of complete chloroplast genome sequences of four early-diverging angiosperms: Buxus (Buxaceae), Chloranthus (Chloranthaceae), Dioscorea (Dioscoreaceae), and Illicium (Schisandraceae). Mol Phylogenet Evol 2007, 45(2):547-563.
64. Kim YK, Park CW, Kim KJ: Complete chloroplast DNA sequence from a Korean endemic genus, Megaleranthis saniculifolia, and its evolutionary implications. Mol Cells 2009, 27(3):365-381.
65. Sun YX, Moore MJ, Meng AP, Soltis PS, Soltis DE, Li JQ, Wang HC: Complete plastid genome sequencing of Trochodendraceae reveals a significant expansion of the inverted repeat and suggests a Paleogene divergence between the two extant species. PLoS One 2013, 8(4):e60429.
66. Zhong B, Yonezawa T, Zhong Y, Hasegawa M: Episodic evolution and adaptation of chloroplast genomes in ancestral grasses. PLoS One 2009, 4(4):e5297.
67. Drew BT, Ruhfel BR, Smith SA, Moore MJ, Briggs BG, Gitzendanner MA, Soltis PS, Soltis DE: Another look at the root of the angiosperms reveals a familiar tale. Syst Biol 2014, 63(3):368-382.
68. Ruhfel BR, Gitzendanner MA, Soltis PS, Soltis DE, Burleigh JG: From algae to angiosperms-inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol Biol 2014, 14:23.
69. Bergsten J: A review of long-branch attraction. Cladistics 2005, 21(2):163-193.
70. Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM: Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol 2008, 8:36.
71. Jia RZ, Ming R, Zhu YJ: Genome-wide analysis of Nucleotide-Binding Site (NBS) disease Resistance (R) Genes in Sacred Lotus (Nelumbo nucifera Gaertn.) reveals their transition role during early evolution of land plants. Tropical Plant Biol 2013, 6(2-3):98-116.
72. Li JK, Zhou EX, Li DX, Huang SQ: Multiple northern refugia for Asian sacred lotus, an aquatic plant with characteristics of ice-age endurance. Aust J Bot 2010, 58(6):463-472.
73. Jansen RK, Raubeson LA, Boore JL, de Pamphilis CW, Chumley TW, Haberle RC, Wyman SK, Alverson AJ, Peery R, Herman SJ, Fourcade HM, Kuehl JV, McNeal JR, Leebens-Mack J, Cui LY: Methods for obtaining and analyzing whole chloroplast genome sequences. Method Enzymol 2005, 395:348-384.
74. Wyman SK, Jansen RK, Boore JL: Automatic annotation of organellar genomes with DOGMA. Bioinformatics 2004, 20(17):3252-3255.
75. 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(Web Server issue):W686-W689.
76. Conant GC, Wolfe KH: GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 2008, 24(6):861-862.
77. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739.
78. Xia X, Xie Z: DAMBE: software package for data analysis in molecular biology and evolution. J Hered 2001, 92(4):371-373.
79. Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14(9):817-818.
80. Stamatakis A, Hoover P, Rougemont J: A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 2008, 57(5):758-771.
81. Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
82. dos Reis M, Yang Z: Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol Biol Evol 2011, 28(7):2161-2172.
83. Rannala B, Yang Z: Inferring speciation times under an episodic molecular clock. Syst Biol 2007, 56(3):453-466.
84. Yang Z: Computational Molecular Evolution. Oxford: Oxford University Press; 2006.
85. Yang Z, Rannala B: Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds. Mol Biol Evol 2006, 23(1):212-226.