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PLOS ONE  2011 

High-Throughput Sequencing of Six Bamboo Chloroplast Genomes: Phylogenetic Implications for Temperate Woody Bamboos (Poaceae: Bambusoideae)

DOI: 10.1371/journal.pone.0020596

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Abstract:

Background Bambusoideae is the only subfamily that contains woody members in the grass family, Poaceae. In phylogenetic analyses, Bambusoideae, Pooideae and Ehrhartoideae formed the BEP clade, yet the internal relationships of this clade are controversial. The distinctive life history (infrequent flowering and predominance of asexual reproduction) of woody bamboos makes them an interesting but taxonomically difficult group. Phylogenetic analyses based on large DNA fragments could only provide a moderate resolution of woody bamboo relationships, although a robust phylogenetic tree is needed to elucidate their evolutionary history. Phylogenomics is an alternative choice for resolving difficult phylogenies. Methodology/Principal Findings Here we present the complete nucleotide sequences of six woody bamboo chloroplast (cp) genomes using Illumina sequencing. These genomes are similar to those of other grasses and rather conservative in evolution. We constructed a phylogeny of Poaceae from 24 complete cp genomes including 21 grass species. Within the BEP clade, we found strong support for a sister relationship between Bambusoideae and Pooideae. In a substantial improvement over prior studies, all six nodes within Bambusoideae were supported with ≥0.95 posterior probability from Bayesian inference and 5/6 nodes resolved with 100% bootstrap support in maximum parsimony and maximum likelihood analyses. We found that repeats in the cp genome could provide phylogenetic information, while caution is needed when using indels in phylogenetic analyses based on few selected genes. We also identified relatively rapidly evolving cp genome regions that have the potential to be used for further phylogenetic study in Bambusoideae. Conclusions/Significance The cp genome of Bambusoideae evolved slowly, and phylogenomics based on whole cp genome could be used to resolve major relationships within the subfamily. The difficulty in resolving the diversification among three clades of temperate woody bamboos, even with complete cp genome sequences, suggests that these lineages may have diverged very rapidly.

References

[1]  Janzen DH (1976) Why bamboos wait so long to flower. Ann Rev Ecol Syst 7: 347–391.
[2]  INBAR (1999) Socio-economic Issues and Constraints in the Bamboo and Rattan Sectors: International Network for Bamboo and Rattan's Assessment. Beijing.
[3]  Judziewicz EJ, Clark LG, Londono X, Stern MJ (1999) American Bamboos. Washington, DC: Smithsonian Institution Press.
[4]  Bystriakova N, Kapos V, Stapleton C, Lysenko I (2003) Bamboo biodiversity: Information for planning conservation and management in the Asia-Pacific region. UNEP-WCMC/INBAR.
[5]  Bystriakova N, Kapos V, Lysenko I (2004) Bamboo biodiversity: Africa, Madagascar and the Americas. UNEP-WCMC/INBAR.
[6]  Li DZ, Wang ZP, Zhu ZD, Xia NH, Jia LZ, et al. (2006) Bambuseae. In: Wu ZY, Raven PH, editors. Flora of China. Vol. 22. Beijing & St. Louis: Science Press & Missouri Botanical Garden Press.
[7]  Renvoize SA, Clayton WD (1992) Classification and evolution of grasses. In: Chapman GP, editor. Grass Evolution and Domestication. Cambridge: Cambridge University Press.
[8]  Grass Phylogeny Working Group [Barker NP, Clark LG, Davis JI, Duvall MR, Guala GF, et al.] (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88: 373–457.
[9]  Sanchen-Ken JG, Clark LG, Kellogg EA, Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Syst Bot 32: 71–80.
[10]  Bouchenak-Khelladi Y, Salamin N, Savolainen V, Forest F, Bank M, et al. (2008) Large multi-gene phylogenetic trees of the grasses (Poaceae): progress towards complete tribal and generic level sampling. Mol Phylogenet Evol 47: 488–505.
[11]  Zhang W (2000) Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data. Mol Phylogenet Evol 15: 135–146.
[12]  Ohrnberger D (1999) The bamboos of the world: annotated nomenclature and literature of the species and the higher and lower taxa. Amsterdam: Elsevier Science.
[13]  Clark LG, Zhang W, Wendel JF (1995) A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst Bot 20: 436–460.
[14]  Sungkaew S, Stapleton CM, Salamin N, Hodkinson TR (2009) Non-monophyly of the woody bamboos (Bambuseae; Poaceae): a multi-gene region phylogenetic analysis of Bambusoideae s.s. J Plant Res 122: 95–108.
[15]  Li DZ (1998) Taxonomy and biogeography of the Bambuseae (Gramineae: Bambusoideae). In: Rao AN, Rao VN, editors. Bamboo Conservation, diversity, ecogeography, germplasm resource utilization and taxonomy. Proceedings of a training course cum workshop. Kunming and Xishuanbanna, Yunnan, China. IPGRI-APO, Serdang, Malaysia.
[16]  Triplett JK, Clark LG (2010) Phylogeny of the Temperate Bamboos (Poaceae: Bambusoideae: Bambuseae) with an Emphasis on Arundinaria and Allies. Syst Bot 35: 102–120.
[17]  Zeng CX, Zhang YX, Triplett JK, Yang JB, Li DZ (2010) Large multi-locus plastid phylogeny of the tribe Arundinarieae (Poaceae: Bambusoideae) reveals ten major lineages and low rate of molecular divergence. Mol Phylogenet Evol 56: 821–839.
[18]  Dyall SD, Brown MT, Johnson PJ (2004) Ancient invasions: from endosymbionts to organelles. Science 304: 253–257.
[19]  Birky CW Jr (1995) Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A 92: 11331–11338.
[20]  Jansen RK, Raubeson LA, Boore JL, dePamphilis CW, Chumley TW, et al. (2005) Methods for obtaining and analyzing whole chloroplast genome sequences. Methods Enzymol 395: 348–384.
[21]  Jansen RK, Cai Z, Raubeson LA, Daniell H, Depamphilis CW, 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 U S A 104: 19369–19374.
[22]  Parks M, Cronn R, Liston A (2009) Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biol 7: 84.
[23]  Moore MJ, Soltis PS, Bell CD, Burleigh JG, Soltis DE (2010) Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci U S A 107: 4623–4628.
[24]  Shendure J, Ji H (2008) Next-generation DNA sequencing. Nat Biotechnol 26: 1135–1145.
[25]  Wu FH, Kan DP, Lee SB, Daniell H, Lee YW, et al. (2009) Complete nucleotide sequence of Dendrocalamus latiflorus and Bambusa oldhamii chloroplast genomes. Tree Physiol 29: 847–856.
[26]  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.
[27]  Cronn R, Liston A, Parks M, Gernandt DS, Shen R, et al. (2008) Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucleic Acids Res 36: e122.
[28]  Zhong B, Yonezawa T, Zhong Y, Hasegawa M (2009) Episodic evolution and adaptation of chloroplast genomes in ancestral grasses. PLoS One 4: e5297.
[29]  Doyle JJ, Davis JI, Soreng RJ, Garvin D, Anderson MJ (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc Natl Acad Sci U S A 89: 7722–7726.
[30]  Maier RM, Neckermann K, Igloi GL, Kossel H (1995) Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. J Mol Biol 251: 614–628.
[31]  Asano T, Tsudzuki T, Takahashi S, Shimada H, Kadowaki K (2004) Complete nucleotide sequence of the sugarcane (Saccharum officinarum) chloroplast genome: a comparative analysis of four monocot chloroplast genomes. DNA Res 11: 93–99.
[32]  Saski C, Lee SB, Fjellheim S, Guda C, Jansen RK, et al. (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor Appl Genet 115: 571–590.
[33]  Diekmann K, Hodkinson TR, Wolfe KH, van den Bekerom R, Dix PJ, et al. (2009) Complete chloroplast genome sequence of a major allogamous forage species, perennial ryegrass (Lolium perenne L.). DNA Res 16: 165–176.
[34]  Cummings MP, King LM, Kellogg EA (1994) Slipped-strand mispairing in a plastid gene: rpoC2 in grasses (Poaceae). Mol Biol Evol 11: 1–8.
[35]  Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, et al. (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 5: 2043–2049.
[36]  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: 247–261.
[37]  Davis JI, Soreng RJ (2010) Migration of endpoints of two genes relative to boundaries between regions of the plastid genome in the grass family (Poaceae). Am J Bot 97: 874–892.
[38]  Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, et al. (2000) VISTA : visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16: 1046–1047.
[39]  Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, et al. (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29: 4633–4642.
[40]  Timme RE, Kuehl JV, Boore JL, Jansen RK (2007) A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. Am J Bot 94: 302–312.
[41]  Peng ZH, Lu TT, Li LB, Liu XH, Gao ZM, et al. (2010) Genome-wide characterization of the biggest grass, bamboo, based on 10,608 putative full-length cDNA sequences. BMC Plant Biol 10: 116.
[42]  Soltis DE, Albert VA, Sarolainen V, Hilu K, Qiu YL, et al. (2004) Genome-scale data, angiosperm relationships, and ‘ending incongrurnce’: a cautionary tale in phylogenetics. Trends Plant Sci 9: 477–483.
[43]  Yang JB, Yang HQ, Li DZ, Wong KM, Yang YM (2010) Phylogeny of Bambusa and its allies (Poaceae: Bambusoideae) inferred from nuclear GBSSI gene and plastid psbA-trnH, rpl32-trnL and rps16 intron DNA sequences. Taxon 59: 1102–1110.
[44]  Sun Y, Xia N, Lin R (2005) Phylogenetic analysis of Bambusa (Poaceae: Bambusoideae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. Biochem Genet 43: 603–612.
[45]  Yang HQ, Yang JB, Peng ZH, Gao J, Yang YM, et al. (2008) A molecular phylogenetic and fruit evolutionary analysis of the major groups of the paleotropical woody bamboos (Gramineae: Bambusoideae) based on nuclear ITS, GBSSI gene and plastid trnL-F DNA sequences. Mol Phylogenet Evol 48: 809–824.
[46]  Triplett JK, Oltrogge KA, Clark LG (2010) Phylogenetic relationships and natural hybridization among the North American woody bamboos (Poaceae: Bambusoideae: Arundinaria). Am J Bot 97: 471–492.
[47]  Clark LG, Davidse G, Ellis RP (1989) Natural hybridization in bamboos: evidence from Chusquea sect. Swallenochloa (Poaceae: Bambusoideae). Nat Geogr Res 5: 459–476.
[48]  Bapteste E, Philippe H (2002) The potential value of indels as phylogenetic markers: position of trichomonads as a case study. Mol Biol Evol 19: 972–977.
[49]  Egan AN, Crandall KA (2008) Incorporating gaps as phylogenetic characters across eight DNA regions: ramifications for North American Psoraleeae (Leguminosae). Mol Phylogenet Evol 46: 532–546.
[50]  Smith SA, Donoghue MJ (2008) Rates of molecular evolution are linked to life history in flowering plants. Science 322: 86–89.
[51]  Gaut BS, Clark LG, Wendel JF, Muse SV (1997) Comparisons of the molecular evolutionary process at rbcL and ndhF in the grass family (Poaceae). Mol Biol Evol 14: 769–777.
[52]  Gong X, Zeng F, Yan L (1994) An efficient method for the purification of chloroplast DNA from higher plants. J Wuhan Bot Res 12: 277–280.
[53]  Li R, Zhu H, Ruan J, Qian W, Fang X, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 265–272.
[54]  Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
[55]  Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20: 3252–3255.
[56]  Goremykin VV, Holland B, Hirsch-Ernst KI, Hellwig FH (2005) Analysis of Acorus calamus chloroplast genome and its phylogenetic implications. Mol Biol Evol 22: 1813–1822.
[57]  Hansen DR, Dastidar SG, Cai Z, Penaflor C, Kuehl JV, et al. (2007) 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 45: 547–563.
[58]  Mardanov AV, Ravin NV, Kuznetsov BB, Samigullin TH, Antonov AS, et al. (2008) Complete sequence of the duckweed (Lemna minor) chloroplast genome: structural organization and phylogenetic relationships to other angiosperms. J Mol Evol 66: 555–564.
[59]  Wu FH, Chan MT, Liao DC, Hsu CT, Lee YW, et al. (2010) Complete chloroplast genome of Oncidium Gower Ramsey and evaluation of molecular markers for identification and breeding in Oncidiinae. BMC Plant Biol 10: 68.
[60]  Chang CC, Lin HC, Lin IP, Chow TY, Chen HH, 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: 279–291.
[61]  Guisinger MM, Chumley TW, Kuehl JV, Boore JL, Jansen RK (2010) Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. J Mol Evol 70: 149–166.
[62]  Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511–518.
[63]  Swofford DL (2002) PAUP: phylogenetic analysis using parsimony, version 4.0 b10. Sunderland, MA: Sinauer Associates.
[64]  Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.
[65]  Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
[66]  Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53: 793–808.
[67]  Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817–818.
[68]  Gielly L, Taberlet P (1994) The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. Mol Biol Evol 11: 769–777.
[69]  Morris LM, Duvall MR (2010) The chloroplast genome of Anomochloa marantoidea (Anomochlooideae; Poaceae) comprises a mixture of grass-like and unique features. Am J Bot 97: 620–627.
[70]  Leseberg CH, Duvall MR (2009) The complete chloroplast genome of Coix lacryma-jobi and a comparative molecular evolutionary analysis of plastomes in cereals. J Mol Evol 69: 311–318.
[71]  Calsa Junior T, Carraro DM, Benatti MR, Barbosa AC, Kitajima JP, et al. (2004) Structural features and transcript-editing analysis of sugarcane (Saccharum officinarum L.) chloroplast genome. Curr Genet 46: 366–373.
[72]  Bortiri E, Coleman-Derr D, Lazo GR, Anderson OD, Gu YQ (2008) The complete chloroplast genome sequence of Brachypodium distachyon: sequence comparison and phylogenetic analysis of eight grass plastomes. BMC Res Notes 1: 61.
[73]  Cahoon AB, Sharpe RM, Mysayphonh C, Thompson EJ, Ward AD, et al. (2010) The complete chloroplast genome of tall fescue (Lolium arundinaceum; Poaceae) and comparison of whole plastomes from the family Poaceae. Am J Bot 97: 49–58.
[74]  Diekmann K, Hodkinson TR, Fricke E, Barth S (2008) An optimized chloroplast DNA extraction protocol for grasses (Poaceae) proves suitable for whole plastid genome sequencing and SNP detection. PLoS One 3: e2813.
[75]  Ogihara Y, Isono K, Kojima T, Endo A, Hanaoka M, et al. (2002) Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA. Mol Genet Genomics 266: 740–746.
[76]  Shahid Masood M, Nishikawa T, Fukuoka S, Njenga PK, Tsudzuki T, et al. (2004) The complete nucleotide sequence of wild rice (Oryza nivara) chloroplast genome: first genome wide comparative sequence analysis of wild and cultivated rice. Gene 340: 133–139.
[77]  Tang J, Xia H, Cao M, Zhang X, Zeng W, et al. (2004) A comparison of rice chloroplast genomes. Plant Physiol 135: 412–420.
[78]  Hiratsuka J, Shimada H, Whittier R, Ishibashi T, Sakamoto M, et al. (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet 217: 185–194.

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