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Comparative Analysis of Asteraceae Chloroplast Genomes: Structural Organization, RNA Editing and Evolution

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Abstract

Comparative chloroplast genome analysis presents new opportunities for performing molecular phylogeny studies and revealing the significant evolutionary features in higher plants, which has been widely documented from conifers to grass family. However, a systematic analysis of chloroplast genomes in Asteraceae family has not been conducted up to now. In this study, we compared and analyzed the gene content, genomic organization, and RNA editing sites of eight representative Asteraceae chloroplast genomes. Results showed that Asteraceae chloroplast had relatively conservative gene content. No gain or loss events occurred in the protein-coding genes, while some differences were found to be present in the gene structure and transfer RNA (tRNA) abundance. Genome structure analysis found some Asteraceae-specific or species-specific structure variations, and sequence rearrangement events were present in these genomes, suggesting specific evolutionary processes have occurred in this family. Some DNA regions containing parsimony-informative characters higher than 5 % were also identified, which could be used as the new molecular markers for phylogenetic analysis and plant identification of Asteraceae species. Furthermore, RNA editing in these genomes was investigated through computational analysis, and some species-specific sites were identified. Finally, phylogenetic analysis of 81 genes from 70 species supported the monophyly of the Asteraceae. Our study for the first time compared the organization, structure, and sequence divergence of eight Asteraceae chloroplast genomes, which will provide the valuable resource for molecular phylogeny of Asteraceae species and also facilitate the genetic and evolutionary studies in this family.

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References

  • Barker MS, Kane NC, Matvienko M, Kozik A, Michelmore RW, Knapp SJ, Rieseberg LH (2008) Multiple paleopolyploidizations during the evolution of the compositae reveal parallel patterns of duplicate gene retention after millions of years. Mol Biol Evol 25:2445–2455. doi:10.1093/molbev/msn187

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bock DG, Kane NC, Ebert DP, Rieseberg LH (2014) Genome skimming reveals the origin of the Jerusalem artichoke tuber crop species: neither from Jerusalem nor an artichoke. New Phytol 201:1021–1030

    Article  CAS  PubMed  Google Scholar 

  • Bremer K (1994) Asteraceae: cladistics and classification. Timber Press, Portland

    Google Scholar 

  • Carlquist S (1976) Tribal interrelationships and phylogeny of the Asteraceae. Aliso 8:465–492

    Google Scholar 

  • Chen H, Deng L, Jiang Y, Lu P, Yu J (2011) RNA editing sites exist in protein-coding genes in the chloroplast genome of Cycas taitungensis. J Integr Plant Biol 53:961–970. doi:10.1111/j.1744-7909.2011.01082.x

    Article  CAS  PubMed  Google Scholar 

  • Chumley TW, Palmer JD, Mower JP, Fourcade HM, Calie PJ, Boore JL, Jansen RK (2006) The complete chloroplast genome sequence of Pelargonium × hortorum: organization and evolution of the largest and most highly rearranged chloroplast genome of land plants. Mol Biol Evol 23:2175–2190. doi:10.1093/molbev/msl089

    Article  CAS  PubMed  Google Scholar 

  • Chung HJ, Jung JD, Park HW, Kim JH, Cha HW, Min SR, Jeong WJ, Liu JR (2006) The complete chloroplast genome sequences of Solanum tuberosum and comparative analysis with Solanaceae species identified the presence of a 241-bp deletion in cultivated potato chloroplast DNA sequence. Plant Cell Rep 25:1369–1379. doi:10.1007/s00299-006-0196-4

    Article  CAS  PubMed  Google Scholar 

  • Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. doi:10.1101/gr.2289704

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dempewolf H, Kane NC, Ostevik KL et al (2010) Establishing genomic tools and resources for Guizotia abyssinica (L.f.) Cass.—the development of a library of expressed sequence tags, microsatellite loci, and the sequencing of its chloroplast genome. Mol Ecol Resour 10:1048–1058. doi:10.1111/j.1755-0998.2010.02859.x

    Article  CAS  PubMed  Google Scholar 

  • Doorduin L, Gravendeel B, Lammers Y, Ariyurek Y, Chin-A-Woeng T, Vrieling K (2011) The complete chloroplast genome of 17 individuals of pest species Jacobaea vulgaris: SNPs, microsatellites and barcoding markers for population and phylogenetic studies. DNA Res 18:93–105. doi:10.1093/dnares/dsr002

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279. doi:10.1093/nar/gkh458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Funk VA, Bayer RJ, Keeley S et al (2005) Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. In: Friis I, Balslev H (eds) Plant diversity and complexity patterns: local, regional and global dimensions, the Royal Danish Academy of Sciences and Letters in Copenhagen. Denmark, Kgl. Danske Videnskabernes Selskab, pp 343–373

    Google Scholar 

  • Ghimiray D, Sharma BC (2014) Comparative and bioinformatics analyses of the solanaceae chloroplast genomes: plastome organization is more or less conserved at family level. J App Biol Biotech 3:021–026. doi:10.7324/JABB.2014.2305

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95–98

    CAS  Google Scholar 

  • Howe CJ, Barbrook AC, Koumandou VL, Nisbet RER, Symington HA, Wightman TF (2003) Evolution of the chloroplast genome. Philos Trans R Soc Lond B Biol Sci 358:99–107. doi:10.1098/rstb.2002.1176

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jansen RK, Cai ZQ, Raubeson LA 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 104:19369–19374. doi:10.1073/pnas.0709121104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim K-J, Choi K-S, Jansen RK (2005) Two chloroplast DNA inversions originated simultaneously during the early evolution of the sunflower family (Asteraceae). Mol Biol Evol 22:1783–1792. doi:10.1093/molbev/msi174

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Huo N, Dong L et al (2013) Complete chloroplast genome sequences of Mongolia medicine Artemisia frigida and phylogenetic relationships with other plants. PLoS ONE 8:e57533. doi:10.1371/journal.pone.0057533

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lundberg J, Bremer K (2003) A phylogenetic study of the order Asterales using one morphological and three molecular data sets. Int J Plant Sci 164:553–578. doi:10.1086/374829

    Article  CAS  Google Scholar 

  • Maier RM, Neckermann K, Igloi GL, Kössel 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. doi:10.1006/jmbi.1995.0460

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp 1-8. doi:10.1109/GCE.2010.5676129

  • Mower JP (2009) The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res 37:W253–W259. doi:10.1093/nar/gkp337

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nie X, Lv SZ, Zhang YX et al (2012) Complete chloroplast genome sequence of a major invasive species, crofton weed (Ageratina adenophora). PLoS ONE 7:e36869. doi:10.1371/journal.pone.0036869

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nie XJ, Deng PC, Feng KW et al (2014) Comparative analysis of codon usage patterns in chloroplast genomes of the Asteraceae family. Plant Mol Biol Report 32:828–840

    Article  CAS  Google Scholar 

  • Ogihara Y, Terachi T, Sasakuma T (1988) Intramolecular recombination of chloroplast genome mediated by short direct-repeat sequences in wheat species. Proc Natl Acad Sci 85:8573–8577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ovcharenko I, Loots GG, Giardine BM, Hou M, Ma J, Hardison RC, Stubbs L, Miller W (2005) Mulan: multiple-sequence local alignment and visualization for studying function and evolution. Genome Res 15:184–194. doi:10.1101/gr.3007205

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Palmer JD (1991) Plastid chromosomes: structure and evolution. In: Hermann RG (ed) The molecular biology of plastids, vol 7A, Cell culture and somatic cell genetics of plants. Springer, Vienna, pp 5–53

    Chapter  Google Scholar 

  • Raubeson LA, Jansen RK (2005) Chloroplast genomes of plants. In: Herry RJ (ed) Plant diversity and evolution: genotypic and phenotypic variation in higher plants. CABI Publising, Wallingford, pp 45–68

    Chapter  Google Scholar 

  • Rivas JDL, Lozano JJ, Ortiz AR (2002) Comparative analysis of chloroplast genomes: functional annotation, genome-based phylogeny, and deduced evolutionary patterns. Genome Res 12:567–583. doi:10.1101/gr.209402

    Article  PubMed Central  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M et al (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J 9:2043–2049

    Google Scholar 

  • Swofford DL (2002) PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts

  • Tillich M, Lehwark P, Morton BR, Maier UG (2006) The evolution of chloroplast RNA editing. Mol Biol Evol 23:1912–1921

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.3732/ajb.94.3.302

    Article  CAS  PubMed  Google Scholar 

  • Wu CS, Lin CP, Hsu CY, Wang RJ, Chaw SM (2011) Comparative chloroplast genomes of pinaceae: insights into the mechanism of diversified genomic organizatio ns. Genome Biol Evol 3:309–319

Download references

Acknowledgments

This research was mainly funded by the National Basic Research Program of China (973 Program) (Grant No. 2009CB119200) and the National Natural Science Foundation of China (Grant No. 31471825) and partially supported by 948 Program (Grant No. 2010-S1), Ministry of Agriculture of China and the Open Project Program (Grant No. SKLOF201314), State Key Laboratory for Biology of Plant Diseases and Insect Pest.

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Correspondence to Song Weining or Xiaojun Nie.

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Mengxing Wang and Licao Cui contributed equally to this work.

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(DOC 192 kb)

ESM_4

Dot-plot comparison showing conserved and inverted regions found in two Chrysanthemum species, Ageratina, Guizotia, Helianthus, Jacobaea and Lactuca cp genomes (JPEG 941 kb)

ESM_5

Phylogenetic tree reconstruction of 70 taxa using maximum likelihood (ML) based on concatenated sequence from 81 cp genes. The position of the Asteraceae family is indicated by a red box (JPEG 1697 kb)

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Wang, M., Cui, L., Feng, K. et al. Comparative Analysis of Asteraceae Chloroplast Genomes: Structural Organization, RNA Editing and Evolution. Plant Mol Biol Rep 33, 1526–1538 (2015). https://doi.org/10.1007/s11105-015-0853-2

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