Thirteen Camellia chloroplast genome sequences determined by high-throughput sequencing: genome structure and phylogenetic relationships

BMC Evolutionary Biology

Li-Zhi Gao¹  Shu-Yan Mao¹  Yuan Liu²  Chao Shi²  Hui Huang¹ 

[1] Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species in Southwest China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China;University of the Chinese Academy of Sciences, Beijing 100039, China

关键词: Taxonomic identification;    Genomic structure;    Phylogenetic relationships;    Chloroplast genome;    Camellia;   

Others  :  855097
DOI  :  10.1186/1471-2148-14-151

 received in 2014-01-01, accepted in 2014-06-20,  发布年份 2014

【 摘 要 】

Background

Camellia is an economically and phylogenetically important genus in the family Theaceae. Owing to numerous hybridization and polyploidization, it is taxonomically and phylogenetically ranked as one of the most challengingly difficult taxa in plants. Sequence comparisons of chloroplast (cp) genomes are of great interest to provide a robust evidence for taxonomic studies, species identification and understanding mechanisms that underlie the evolution of the Camellia species.

Results

The eight complete cp genomes and five draft cp genome sequences of Camellia species were determined using Illumina sequencing technology via a combined strategy of de novo and reference-guided assembly. The Camellia cp genomes exhibited typical circular structure that was rather conserved in genomic structure and the synteny of gene order. Differences of repeat sequences, simple sequence repeats, indels and substitutions were further examined among five complete cp genomes, representing a wide phylogenetic diversity in the genus. A total of fifteen molecular markers were identified with more than 1.5% sequence divergence that may be useful for further phylogenetic analysis and species identification of Camellia. Our results showed that, rather than functional constrains, it is the regional constraints that strongly affect sequence evolution of the cp genomes. In a substantial improvement over prior studies, evolutionary relationships of the section Thea were determined on basis of phylogenomic analyses of cp genome sequences.

Conclusions

Despite a high degree of conservation between the Camellia cp genomes, sequence variation among species could still be detected, representing a wide phylogenetic diversity in the genus. Furthermore, phylogenomic analysis was conducted using 18 complete cp genomes and 5 draft cp genome sequences of Camellia species. Our results support Chang’s taxonomical treatment that C. pubicosta may be classified into sect. Thea, and indicate that taxonomical value of the number of ovaries should be reconsidered when classifying the Camellia species. The availability of these cp genomes provides valuable genetic information for accurately identifying species, clarifying taxonomy and reconstructing the phylogeny of the genus Camellia.

【 授权许可】

   
2014 Huang et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Vijayan K, Zhang WJ, Tsou CH: Molecular taxonomy of Camellia (Theaceae) inferred from nrITS sequences. Am J Bot 2009, 96:1348-1360.
• [2]Min TL, Bruce B: Flora of China. Beijing, China: Science Press; 2010.
• [3]Wachira FN, Tanaka J, Takeda Y: Genetic variation and differentiation in tea (Camellia sinensis) germplasm revealed by RAPD and AFLP variation. J Hort Sci Biotech 2001, 76:557-563.
• [4]Wang LY, Liu BY, Jiang YY, Duan YS, Cheng H, Zhou J, Tang YC: Phylogenetic analysis of inter species in section Thea through SSR markers. J Tea Sci 2009, 29:341-346.
• [5]Chen L, Yamaguchi S, Wang PS, Xu M, Song WX, Tong QQ: Genetic polymorphism and molecular phylogeny analysis of section Thea based on RAPD markers. J Tea Sci 2002, 22:19-24.
• [6]Ji PZ, Wang YG, Zhang J, Tang YC, Huang XQ, Wang PS: Genetic relationships between sect. Thea from Yunnan province revealed by inter-simple sequence repeat polymerase China reaction. Southwest China J Agric Sci 2009, 22:584-588.
• [7]Tian M, Li JY, Ni S, Fan ZQ, Li XL: Phylogenetic study on section Camellia based on ITS sequences data. Acta Hort Sin 2008, 35:1685-1688.
• [8]Fang W, Yang JB, Yang SX, Li DZ: Phylogeny of Camellia sects. Longipedicellata, Chrysantha and Longissima (Theaceae) based on sequence data of four chloroplast DNA Loci. Acta Bot Yunnanica 2010, 32:1-13.
• [9]Yang JB, Yang SX, Li HT, Yang J, Li DZ: Comparative chloroplast genomes of Camellia species. PLoS ONE 2013, 8:e73053.
• [10]McCauley DE, Stevens JE, Peroni PA, Raveill JA: The spatial distribution of chloroplast DNA and allozyme polymorphisms within a population of Silene alba (Caryophyllaceae). Am J Bot 1996, 83:727-31.
• [11]Small RL, Cronn RC, Wendel JF: Use of nuclear genes for phylogeny reconstruction in plants. Aust Syst Bot 2004, 17:145-70.
• [12]Jansen RK, Cai Z, Raubeson LA, Daniell H, de Pamphilis CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee S, Peery R, McNeal JR, Kuehl J, 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, 104:19369-19374.
• [13]Parks M, Cronn R, Liston A: Increasing phylogenetic resolution at low taxonomic levels using massively parallel sequencing of chloroplast genomes. BMC Biol 2009, 7:84.
• [14]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, 107:4623-4628.
• [15]Huang H, Tong Y, Zhang QJ, Gao LZ: Genome Size Variation among and within Camellia Species by Using Flow Cytometric Analysis. PLoS ONE 2013, 8:e64981.
• [16]Liu Y, Yang SX, Ji PZ, Gao LZ: Phylogeography of Camellia taliensis (Theaceae) inferred from chloroplast and nuclear DNA: insights into evolutionary history and conservation. BMC Evol Biol 2012, 12:92-105.
• [17]Provan J, Powell W, Hollingsworth PM: Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 2001, 16:142-147.
• [18]Shi C, Liu Y, Huang H, Xia EH, Zhang HB, Gao LZ: Contradiction between plastid gene transcription and function due to complex posttranscriptional splicing: an exemplary study of ycf15 function and evolution in angiosperms. PLoS ONE 2013, 8:e59620.
• [19]Cronn R, Liston A, Parks M, Gernandt DS, Shen RK: Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by- synthesis technology. Nucleic Acids Res 2008, 36:e122.
• [20]Matsuoka Y, Yamazaki Y, Ogihara Y, Tsunewaki K: Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. Mol Biol Evol 2002, 19:2084-2091.
• [21]Xu Q, Xiong GJ, Li PB, He F, Huang Y, Wang KB, Li ZH, Hua JP: Analysis of Complete Nucleotide Sequences of 12 Gossypium Chloroplast Genomes: Origin and Evolution of Allotetraploids. PLoS ONE 2012, 7:e37128.
• [22]Davis JI, Soreng RJ: Migration of endpoints of two genes relative to boundaries between regions of the plastid genome in the grass family (Poaceae). Am J Bot 2010, 97:874-892.
• [23]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, 11:247-261.
• [24]Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I: VISTA : visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 2000, 16:1046-1047.
• [25]Palmer JD: Plastid chromosomes: structure and evolution. In the Molecular Biology of Plastids. Edited by Bogorad L, Vasil IK. New York: Academic Press; 1991:5-53.
• [26]Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R: REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 2001, 29:4633-4642.
• [27]Saski C, Lee SB, Fjellheim S, Guda C, Jansen RK, Luo H, Tomkins J, Rognli OA, Daniell H, Clarke JL: Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor Appl Genet 2007, 115:571-590.
• [28]Zhang YJ, Ma PF, Li DZ: High-throughput sequencing of six bamboo chloroplast genomes: phylogenetic implications for temperate woody bamboos (Poaceae: Bambusoideae). PLoS ONE 2011, 6:e20596.
• [29]Tangphatsornruang S, Sangsrakru D, Chanprasert J, Uthaipaisanwong P, Yoocha T, Jomchai N, Tragoonrung S: The chloroplast genome sequence of Mungbean (Vigna radiata) determined by high-throughput pyrosequencing: structural organization and phylogenetic relationship. DNA Res 2010, 17:11-22.
• [30]Asano T, Tsudzuki T, Takahashi S, Shimada H, Kadowaki K: Complete nucleotide sequence of the sugarcane (Saccharum officinarum) chloroplast genome: A comparative analysis of four monocot chloroplast genomes. DNA Res 2004, 11:93-99.
• [31]Timme RE, Kuehl JV, Boore JL, Jansen RK: A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: Identification of divergent regions and categorization of shared repeats. Am J Bot 2007, 94:302-312.
• [32]Cavalier-Smith T: Chloroplast evolution: secondary symbiogenesis and multiple losses. Curr Biol 2002, 12:62-64.
• [33]Gao L, Yi X, Yang YX, Su YJ, Wang T: Complete chloroplast genome sequence of a tree fern Alsophila spinulosa: insights into evolutionary changes in fern chloroplast genomes. BMC Evol Biol 2009, 9:130-144.
• [34]Echt CS, DeVerno LL, Anzidei M, Vendramin GG: Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Mol Ecol 1998, 7:307-316.
• [35]Powell W, Morgante M, Andre C, Mcnicol JW, Machray GC, Doyle JJ, Tingey SV, Rafalski JA: Hypervariable microsatellites provide a general source of polymorphic DNA markers for the chloroplast genome. Curr Biol 1995, 5:1023-1029.
• [36]Kuang DY, Wu H, Wang YL, Gao LM, Zhang SZ, Lu L: Complete chloroplast genome sequence of Magnolia kwangsiensis (Magnoliaceae): implication for DNA barcoding and population genetics. Genome 2011, 54:663-673.
• [37]Yi D-K, Kim K-J: Complete Chloroplast Genome Sequences of Important Oilseed Crop Sesamum indicum L. PLoS ONE 2012, 7:e35872.
• [38]Jakobsson M, Sall T, Lind-Hallden C, Hallden C: Evolution of chloroplast mononucleotide microsatellites in Arabidopsis thaliana. Theor Appl Genet 2007, 114:223-235.
• [39]Garris AJ, Tai TH, Coburn J, Kresovich S, McCouch S: Genetic structure and diversity in Oryza sativa L. Genetics 2005, 169:1631-1638.
• [40]Xu DH, Abe J, Gai JY, Shimamoto Y: Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean. Theor Appl Genet 2002, 105:645-653.
• [41]Leseberg CH, Duvall MR: The complete chloroplast genome of Coix lacryma-jobi and a comparative molecular evolutionary analysis of plastomes in cereals. J Mol Evol 2009, 69:311-318.
• [42]Grover CE, Yu Y, Wing RA, Paterson AH, Wendel JF: A phylogenetic analysis of indel dynamics in the cotton genus. Mol Biol Evol 2008, 25:1415-1428.
• [43]Britten RJ, Rowen L, Williams J, Cameron RA: Majority of divergence between closely related DNA samples is due to indels. Proc Natl Acad Sci U S A 2003, 100:4661-4665.
• [44]Chen JQ, Wu Y, Yang H, Bergelson J, Kreitman M, Tian D: Variation in the ratio of nucleotide substitution and indel rates across genomes in mammals and bacteria. Mol Biol Evol 2009, 26:1523-1531.
• [45]Yamane K, Yano K, Kawahara T: Pattern and rate of indel evolution inferred from whole chloroplast intergenic regions in sugarcane, maize and rice. DNA Res 2006, 13:197-204.
• [46]McCluskey K, Wiest AE, Grigoriev IV, Lipzen A, Martin J, Schackwitz W, Baker SE: Rediscovery by whole genome sequencing: classical mutations and genome polymorphisms in Neurospora crassa. G3 (Bethesda) 2011, 1:303-316.
• [47]Smith SA, Donoghue MJ: Rates of molecular evolution are linked to life history in flowering plants. Science 2008, 322:86-89.
• [48]Perry AS, Wolfe KH: Nucleotide substitution rates in legume chloroplast DNA depend on the presence of the inverted repeat. J Mol Evol 2002, 55:501-508.
• [49]Clegg MT, Gaut BS, Learn GH, Morton BR: Rates and patterns of chloroplast DNA evolution. Proc Natl Acad Sci U S A 1994, 91:6795-6801.
• [50]Wolfe KH, Gouy ML, Yang YW, Sharp PM, Li WH: Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A 1989, 86:6201-6205.
• [51]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, 104:19363-19368.
• [52]Chang HD, Ren SX: Flora of China. Science Press. Tomus 1998, 49(3):1-251.
• [53]Min TL: A revision of Camellia sect. Thea Acta Bot Yunnanica 1992, 14:115-132.
• [54]Li XH, Zhang CZ, Liu CL, Shi ZP, Luo JW, Chen X: RAPD analysis of the genetic diversity in Chinese tea germplasm. Acta Hort Sin 2007, 34:507-508.
• [55]Peng ZH, Lu TT, Li LB, Liu XH, Gao ZM, Hu T, Yang XW, Feng Q, Guan JP, Weng QJ, Fan DL, Zhu CR, Lu Y, Han B, Jiang ZH: Genome-wide characterization of the biggest grass, bamboo, based on 10,608 putative full-length cDNA sequences. BMC Plant Biol 2010, 10:116-129.
• [56]Bapteste E, Philippe H: The potential value of indels as phylogenetic markers: position of Trichomonads as a case study. Mol Biol Evol 2002, 19:972-977.
• [57]Simmons MP, Ochoterena H, Carr TG: Incorporation, relative homoplasy, and effect of Gap characters in sequence -based phylogenetic analyses. Syst Biol 2001, 50:454-462.
• [58]Shi C, Hu N, Huang H, Gao J, Zhao Y-J, Gao LZ: An Improved Chloroplast DNA Extraction Procedure for Whole Plastid Genome Sequencing. PLoS ONE 2012, 7:e31468.
• [59]Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, Li S, Yang H, Wang J, Wang J: De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 2010, 20:265-272.
• [60]Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A: Geneious v5. 2011., 4Available from http://www.geneious.com
• [61]Wyman SK, Jansen RK, Boore JL: Automatic annotation of organellar genomes with DOGMA. Bioinformatics 2004, 20:3252-3255.
• [62]Lohse M, Drechsel O, Bock R: Organellar Genome DRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet 2007, 52:267-274.
• [63]Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 2005, 33:511-518.
• [64]Thiel T, Michalek W, Varshney RK, Graner A: Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 2003, 106:411-422.
• [65]Gielly L, Taberlet P: The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. Mol Biol Evol 1994, 11:769-777.
• [66]Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.