Abstract
The complete chloroplast genome of Chionographis japonica (Willd.) Maxim. (Melanthiaceae, Liliales) was mapped using polymerase chain reaction and the Sanger method. The circular double-stranded DNA was a typical quadripartite structure consisting of two inverted repeated regions (27,397 bp), a small single copy region (18,205 bp), and a large single-copy region (81,646 bp), with a total length of 154,645 bp. The genome consisted of 137 coding genes, including 91 protein-coding genes, 38 distinct tRNA, and 8 rRNA genes. The ycf15 and ycf68 genes had several internal stop codons interpreted as pseudogenes. The inverted repeat (IR) region expanded to part of the rps3 gene in the junction between large single-copy and IRA regions in C. japonica. We designed 785 primers, of which 481 were used to map the entire chloroplast genome of C. japonica. Primers were compared with the complete chloroplast sequence of Smilax china (Smilacaceae) to identify primers that could be used for other Liliales members and whole chloroplast genome sequencing. Of the primers used for C. japonica, 398 could be used with other smaller species within the order.
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Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410
APG III (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
Asano T, Tsudzuki T, Takahashi S, Shimada H, Kadowaki KI (2004) Complete nucleotide sequence of the sugarcane (Saccharum officinarum) chloroplast genome: a comparative analysis of four monocot chloroplast genomes. DNA Res 11(2):93–99
Bedbrook JR, Bogorad L (1976) Endonuclease recognition sites mapped on Zea mays chloroplast DNA. Proc Natl Acad Sci 73(12):4309–4313
Bedbrook JR, Kolodner R, Bogorad L (1977) Zea mays chloroplast ribosomal RNA genes are part of a 22,000 base pair inverted repeat. Cell 11(4):739–749
Cardle L, Ramsay L, Milbourne D, Macaulay M, Marshall D, Waugh R (2000) Computational and experimental characterization of physically clustered simple sequence repeats in plants. Genetics 156(2):847–854
Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, Chen WH et al (2006) The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol Biol Evol 23(2):279–291
Chase MW, Fay MF, Devey DS, Maurin O, Rønsted N, Davies TJ et al (2006) Multigene analyses of monocot relationships: a summary. Aliso 22:63–75
Chen SC (1980) Chionographis. Flora Reipublicae Popularis Sinicae 14:13–15
Chen SC, Tamura MN (2000) Chionographis. Flora of China 24:88
Conant GC, Wolfe KH (2008) GenomeVX: simple web-based creation of editable circular chromosome maps. Bioinformatics 2:861–862
Daniell H, Kumar S, Dufourmantel N (2005) Breakthrough in chloroplast genetic engineering of agronomically important crops. Trends Biotechnol 23(5):238–245
Davis JI, Stevenson DW, Petersen G, Seberg O, Campbell LM, Freudenstein JV et al (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(3):467–510
Downie SR, Palmer JD (1992) Restriction site mapping of the chloroplast DNA inverted repeat: a molecular phylogeny of the Asteridae. Ann Mo Bot Gard 266–283
Doyle J, Doyle JL (1987) Genomic plant DNA preparation from fresh tissue CTAB method. Phytochem Bull 19(11)
Duvall MR, Clegg MT, Chase MW, Clark WD, Kress WJ, Hills HG et al (1993) Phylogenetic hypotheses for the monocotyledons constructed from rbcL sequence data. Ann Mo Bot Gard 80(3):607–619
Egan AN, Schlueter J, Spooner DM (2012) Applications of next-generation sequencing in plant biology. Am J Bot 99(2):175–185
Erfani J, Ebadi A, Abdollahi H, Fatahi R (2012) Genetic diversity of some pear cultivars and genotypes using simple sequence repeat (SSR) markers. Plant Mol Biol Rep 30:1065–1072
Fay MF, Chase MW, Rønsted N, Devey DS, Pillon Y, Pires JC et al (2006) Phylogenetics of Liliales: summarized evidence from combined analyses of five plastid and one mitochondrial loci. Aliso 22:559–565
FitzSimmons NN, Moritz C, Moore SS (1995) Conservation and dynamics of microsatellite loci over 300 million years of marine turtle evolution. Mol Biol Evol 12(3):432–440
Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 1;32 (Web Server issue):W273-9
Fuse S, Tamura MN (2000) A phylogenetic analysis of the plastid matK gene with emphasis on Melanthiaceae sensu lato. Plant Biol 2(4):415–427
Gantt JS, Baldauf SL, Calie PJ, Weeden NF, Palmer JD (1991) Transfer of rpl22 to the nucleus greatly preceded its loss from the chloroplast and involved the gain of an intron. EMBO J 10(10):3073
Givnish TJ, Ames M, McNeal JR, McKain MR, Steele PR, de Pamphilis CW, Leebens-Mack JH (2010) Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales 1. Ann Mo Bot Gard 97(4):584–616
Goldblatt P (1995) The status of R. Dahlgren’s orders Liliales and Melanthiales. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens, Kew, Richmond, Surrey, UK, pp 181–200
Goremykin VV, Holland B, Hirsch-Ernst KI, Hellwig FH (2005) Analysis of Acorus calamus chloroplast genome and its phylogenetic implications. Mol Biol Evol 22(9):1813–1822
Goulding SE, Wolfe KH, Olmstead RG, Morden CW (1996) Ebb and flow of the chloroplast inverted repeat. Mol Gen Genet MGG 252(1–2):195–206
Hall T (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hara H (1968) A revision of the genus Chionographis (Liliaceae). J Jpn Bot 43:257–288
Harris M, Meyer G, Vandergon J, Vandergon VO (2013) Loss of the acetyl co-A carboxylase (accD) gene in Poales. Plant Mol Biol Rep 31:21–31
Howe CJ, Barbrook AC, Koumandou VL, Nisbet RER, Symington HA, Wightman TF (2003) Evolution of the chloroplast genome. Phil Trans R Soc Land B 358:99–107
Hutchinson J (1934) The families of flowering plants II: monocotyledons. Macmillan Pub, London
Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, Leebens-Mack J et al (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci 104(49):19369–19374
Karp A, Seberg O, Buiatti M (1996) Molecular techniques in the assessment of botanical diversity. Ann Bot 78:143–149
Khan A, Khan I, Heinze B, Azim MK (2012) The chloroplast genome sequence of date palm (Pheonix dactylifera L. cv. ‘Aseel’). Plant Mol Biol Rep 30:666–678
Kim KJ, Lee HL (2004) Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res 11(4):247–261
Kim JS, Hong JK, Chase MW, Fay MF, Kim JH (2013) Familial relationships of the monocot order Liliales based on a molecular phylogenetic analysis using four plastid loci: matK, rbcL, atpB and atpF-H. Bot J Linn Soc 172:5–21
Kim JS, Kim J-H (2013) Comparative genome analysis and phylogenetic relationship of order Liliales insight from the complete plastid genome sequences of two lilies (Lilium longiflorum and Alstroemeria aurea). Plos One 8(6): e68180
Lartillot N, Brinkmann H, Philippe H (2007) Suppression of long-branch attraction artifacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7(Suppl 1):S4
Librado P, Rozas J (2009) DnaSP v5: software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452
Liu J, Qi Z, Zhao Y, Fu C, Xiang Q (2012) Complete cpDNA genome sequence of Smilax china and phylogenetic placement of Liliales—influences of gene partitions and taxon sampling. Mol Phylogenet Evol 64:545–562
Maki M (1992) Fixation indices and genetic diversity in hermaphroditic and gynodioecious populations of Japanese Chionographis (Liliaceae). Heredity 68:329–336
Maki M (1993) Outcrossing and fecundity advantage of females in gynodioecious Chionographis japonica var. kurohimensis (Liliaceae). Am J Bot 80(6):629–634
Maki M, Masuda M (1994) Spatial genetic structure within two populations of a self-incompatible perennial, Chionographis japonica var. japonica (Liliaceae). J Plant Res 107(3):283–287
Meagher TR, Antonovics JJ (1982) Life history variation in dioecious plant populations: a case study of Chamaelirium luteum. Evolution and genetics of life histories. Springer-Verlag, New York, pp 139–154
Millen RS, Olmstead RG, Adams KL, Palmer JD, Lao NT, Heggie L et al (2001) Many parallel losses of infA from chloroplast DNA during angiosperm evolution with multiple independent transfers to the nucleus. Plant Cell Online 13(3):645–658
Narayanan V, Mieczkowski PA, Kim HM, Petes TD, Lobachev KS (2006) The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125(7):1283–1296
Peakall R, Gilmore S, Keys W, Morgante M, Rafalski A (1998) Cross-species amplification of soybean (Glycine max) simple sequence repeats (SSRs) within the genus and other legume genera: implications for the transferability of SSRs in plants. Mol Biol Evol 15(10):1275–1287
Petersen G, Seberg O, Davis JI (2012) Phylogeny of the Liliales (Monocotyledons) with special emphasis on data partition congruence and RNA editing. Cladistics. doi:10.1111/j.1096-0031.2012.00427.x
Primmer CR, Møller AP, Ellegren H (1996) A wide-range survey of cross-species microsatellite amplification in birds. Mol Ecol 5(3):365–378
Raubeson LA, Jansen RK (2005) 4 Chloroplast genomes of plants. In: Henry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI Publishing, London, pp 45–68
Raubeson L, Peery R, Chumley T, Dziubek C, Fourcade HM, Boore J, Jansen R (2007) Comparative chloroplast genomics: analyses including new sequences from the angiosperms Nuphar advena and Ranunculus macranthus. BMC Genomics 8(1):174
Rico C, Rico I, Hewitt G (1996) 470 million years of conservation of microsatellite loci among fish species. Proc R Soc Lond Ser B Biol Sci 263(1370):549–557
Rose O, Falush D (1998) A threshold size for microsatellite expansion. Mol Biol Evol 15(5):613–615
Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386
Rudall PJ, Stobart KL, Hong WP, Conran JG, Funess CA, Kite GC, Chase MW (2000) Consider the lilies: Systematics of Liliales. In: Wilson KL, Morrison DA (eds) Monocots: systematics and evolution. CSIRO: Melbourne, Australia, pp 347–357
Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33(suppl 2):W686–W689
Schmitz-Linneweber C, Maier RM, Alcaraz JP, Cottet A, Herrmann RG, Mache R (2001) The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization. Plant Mol Biol 45(3):307–315
Tamura MN (1998) Melanthiaceae. In: Kubitzki K (ed) The families and genera of vascular plants: monocotyledons vol III. Columbia University Press, New York, NY pp 369–380
Tamura MN, Yamashita J, Fuse S, Haraguchi M (2004) Molecular phylogeny of monocotyledons inferred from combined analysis of plastid matK and rbcL gene sequences. J Plant Res 117(2):109–120
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum-likelihood, evolutionary distance, and maximum-parsimony methods. Mol Biol Evol 28(10):2731–2739
Tanaka NY (1985) Variation of sexual system in Chionographis species. Syuseibutugaku-kenkyu 9:11–19 (In Japanese)
Tanaka N (2003) New status and combinations for Japanese taxa of Chionographis (Melanthiaceae). Novon 13(2):212–215
Tanaka NY, Tanaka N (1977) Chromosome studies in Chionographis (Liliaceae). I. On the holokinetic nature of chromosomes in Chionographis japonica Maxim. Cytol 42:753–763
Tanaka NY, Tanaka N (1979) Chromosome studies in Chionographis (Liliaceae): II. Morphological characteristics of the somatic chromosomes of four Japanese members. Cytol 44:935–949
Terakami S, Matsumura Y, Kurita K, Kanamori H, Katayose Y, Yamamoto T, Katayama H (2012) Complete sequence of the chloroplast genome from pear (Pyrus pyrifolia): genome structure and comparative analysis. Tree Genet Genomics 8(4):841–854
Terrab A, Paun O, Talavera S, Tremetsberger K, Arista M, Stuessy TF (2006) Genetic diversity and population structure in natural populations of Moroccan Atlas cedar (Cedrus atlantica; Pinaceae) determined with cpSSR markers. Am J Bot 93(9):1274–1280
Thurston MI, Field D (2005) Msatfinder: detection and characterisation of microsatellites. Distributed by the authors at http://www.genomics.ceh.ac.uk/msatfinder/. CEH Oxford, Mansfield Road, Oxford OX1 3SR
Vinnersten A, Bremer K (2001) Age and biogeography of major clades in Liliales. Am J Bot 88(9):1695–1703
Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M (1994) Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. Proc Natl Acad Sci 91(21):9794–9798
Wang RJ, Cheng CL, Chang CC, Wu CL, Su TM, Chaw SM (2008) Dynamics and evolution of the inverted repeat-large single copy junctions in the chloroplast genomes of monocots. BMC Evol Biol 8(1):36
Wicker T, Schlagenhauf E, Graner A, Close T, Keller B, Stein N (2006) 454 sequencing put to the test using the complex genome of barley. BMC Genomics 7(1):275
Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci 84(24):9054–9058
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255
Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18
Yang M, Zhang X, Liu G, Yin Y, Chen K, Yun Q et al (2010) The complete chloroplast genome sequence of date palm (Phoenix dactylifera L.). PLoS One 5(9):e12762
Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E et al (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99(2):193–208
Zhang Q, Li J, Zhao Y, Korban SS, Han Y (2012) Evaluation of genetic diversity in Chinese wild apple species along with apple cultivars using SSR markers. Plant Mol Biol Rep 30:539–546
Zomlefer WB (1997) The genera of Melanthiaceae in the southeastern United States. Harv Pap Bot 2:133–177
Zomlefer WB, Williams NH, Whitten WM, Judd WS (2001) Generic circumscription and relationships in the tribe Melanthieae (Liliales, Melanthiaceae), with emphasis on Zigadenus: evidence from ITS and trnL-F sequence data. Am J Bot 88(9):1657–1669
Zomlefer WB, Judd WS, Whitten WM, Williams NH (2006) A synopsis of Melanthiaceae (Liliales) with focus on character evolution in tribe Melanthieae. Aliso 22:566–578
Acknowledgments
We would like to thank Do Hoang Dang Khoa and Sang-Chul Kim of Gachon University for assistance with the analysis and in collection of Chionographis. This study was supported by the National Research Foundation of Korea (NRF) grant fund (MEST 2010–0029131).
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Supplementary Table 1
Primers used for the sequence mapping of C. japonica, separated by region (LSC, SSC, IR) and named according to the appropriate location within the Chionographis sequence. Primers compared with S. china and those with greater than 80 % similarity are listed along with nucleotide position compared with Chionographis (PDF 167 kb)
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Bodin, S.S., Kim, J.S. & Kim, JH. Complete Chloroplast Genome of Chionographis japonica (Willd.) Maxim. (Melanthiaceae): Comparative Genomics and Evaluation of Universal Primers for Liliales. Plant Mol Biol Rep 31, 1407–1421 (2013). https://doi.org/10.1007/s11105-013-0616-x
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DOI: https://doi.org/10.1007/s11105-013-0616-x