Skip to main content
Log in

Phylogenomics, molecular evolution, and estimated ages of lineages from the deep phylogeny of Poaceae

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

The deeply diverging subfamilies of grasses: Anomochlooideae, Pharoideae, and Puelioideae, today inhabit tropical forest floors as sparsely distributed depauperate lineages. The BEP/PACMAD grasses, which make up the majority of the family, are the result of a more recent radiation. Species in the deeply diverging subfamilies were here investigated to better understand molecular evolutionary processes and ages of divergence. Complete chloroplast genomes (plastomes) of Pharus latifolius L., P. lappulaceus Aubl., and Puelia olyriformis (Franch.) Clayton were determined. Four plastome loci from seven species of the deep subfamilies were also sequenced. Phylogenetic and mutation analyses and divergence estimations were conducted on all sequences together with homologous sequences from other Poaceae. Mutation analyses surveyed insertion/deletion mutations across the plastomes, clarified a trend in the molecular evolution of the rpoC2 locus, and indicated unique pseudogenizations in the plastomes of Pharus and Puelia. Phylogenetic analyses largely confirmed earlier multi-gene phylogenies. Phylogenomic and divergence analyses produced estimated origins of the crown nodes of Anomochlooideae at 65–104 Ma, Pharoideae at 44–71 Ma, and Puelioideae at 62–96 Ma. The upper ends of our estimated ranges are in general agreement with previous estimates. However, the lower ends of our ranges are considerably older than previous estimates, reflecting the influence of the less commonly used oldest fossil calibration point. The deeply diverging subfamilies exhibited the accumulation of numerous substitution and indel mutations consistent with a long evolutionary history that predated the radiation of the BEP/PACMAD grasses. We hypothesize that relatively rapid warming and drying in Africa at 55–56.5 Ma may have acted as selective forces stimulating adaptive radiations of grasses from the African tropical forests into diverse habitats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aguirre-Planter E, Jaramillo-Correa J, Gomez-Acevedo S, Khasa D, Bousquet J, Eguiarte L (2012) Phylogeny, diversification rates and species boundaries of Mesoamerican firs (Abies, Pinaceae) in a genus-wide context. Mol Phylogenet Evol 62:263–274. doi:10.1016/j.ympev.2011.09.021

    Article  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi:10.1093/nar/25.17.3389

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Barker N, Linder P, Harley E (1998) Sequences of the grass specific insert in the chloroplast rpoC2 gene elucidate generic relationships of the Arundinoideae (Poaceae). Syst Bot 23:327–350. doi:10.2307/2419509

    Article  Google Scholar 

  • Bouchenak-Khelladi Y, Verboom GA, Savolainen V, Hodkinson TR (2010) Biogeography of the grasses (Poaceae): a phylogenetic approach to reveal evolutionary history in geographical space and geological time. Bot J Linn Soc 162:543–557. doi:10.1111/j.1095-8339.2010.01041.x

    Article  Google Scholar 

  • Bremer K (2002) Gondwanan evolution of the grass alliance of families (Poales). Evol 56:1374–1387. doi:10.1111/j.0014-3820.2002.tb01451.x

    Article  CAS  Google Scholar 

  • Bremer K, Janssen T (2006) Gondwanan origin of major monocot groups inferred from dispersal-vicariance analysis. Aliso 22:22–27

    Google Scholar 

  • Burke SV, Grennan CP, Duvall MR (2012) Plastome sequences of two New World bamboos, Arundinaria gigantea and Cryptochloa strictiflora (Poaceae), extend phylogenomic understanding of Bambusoideae. Am J Bot 99:1951–1961. doi:10.3732/ajb.1200365

    Article  CAS  PubMed  Google Scholar 

  • Chang C–C, Lin H-C, Lin I-P, Chow T-Y, Chen H–H, Chen W-H, Cheng C-H, Lin C-Y, Liu S-M, Chang C–C, Chaw S-M (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. doi:10.1093/molbev/msj029

    Article  CAS  PubMed  Google Scholar 

  • Christin P-A, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43. doi:10.1016/j.cub.2007.11.058

    Article  CAS  PubMed  Google Scholar 

  • Christin P-A, Osborne CP, Chatelet DS, Columbus JT, Besnard G, Hodkinson TR, Garrison LM, Vorontsova MS, Edwards EJ (2013) Anatomical enablers and the evolution of C4 photosynthesis in grasses. Proc Natl Acad Sci USA 110:1381–1386. doi:10.1073/pnas.1216777110

    Article  CAS  PubMed Central  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 

  • Clark LG, Zhang W, Wendel JF (1995) A phylogeny of the grass family (Poaceae) based on ndhF sequence data. Syst Bot 20:436–460. doi:10.2307/2419803

    Article  Google Scholar 

  • Cox MP, Peterson DA, Biggs PJ (2010) SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinf 11:485. doi:10.1186/1471-2105-11-485

    Article  Google Scholar 

  • Cummings M, King L, Kellogg EA (1994) Slipped-strand mispairing in a plastid gene: rpoC2 in grasses (Poaceae). Mol Biol Evol 11:1–8

    CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109

    Article  CAS  PubMed  Google Scholar 

  • Delannoy ES, Fujii C, des Francs C, Brundrett M, Small I (2011) Rampant gene loss in the underground orchid Rhizanthella gardneri highlights evolutionary constraints on plastid genomes. Mol Biol Evol 28:2077–2086. doi:10.1093/molbev/msr028

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dhingra A, Folta K (2005) ASAP: amplification, sequencing and annotation of plastomes. BMC Genom 6:176–189. doi:10.1186/1471-2164-6-176

    Article  Google Scholar 

  • Downie SR, Llanas E, Katz-Downie DS (1996) Multiple independent losses of the rpoC1 intron in angiosperm chloroplast DNAs. Syst Bot 21:135–151. doi:10.2307/2419744

    Article  Google Scholar 

  • Doyle JJ, Davis JI, Soreng RJ, Garvin D, Andersson MJ (1992) Chloroplast DNA inversions and the origin of the grass family (Poaceae). Proc Natl Acad Sci USA 89:7722–7726. doi:10.1073/pnas.89.16.7722

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drabkova L (2002) Comparison of seven DNA extraction and amplification protocols in historical herbarium specimens of Juncaceae. Plant Mol Biol Rep 20:161–175. doi:10.1007/BF02799431

    Article  CAS  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 8:1969. doi:10.1093/molbev/mss075

    Article  Google Scholar 

  • Durbin R, Rice P (1999) Einverted: finds DNA inverted repeats (EMBOSS). European Bioinformatics Institute, Cambridge

    Google Scholar 

  • Duvall MR, Davis JI, Clark LG, Noll JD, Goldman DH, Sánchez-Ken JG (2007) Phylogeny of the grasses (Poaceae) revisited. Aliso 23:237–247

    Article  Google Scholar 

  • Duvall MR, Leseberg CH, Grennan CP, Morris LM (2010) Molecular evolution and phylogenetics of complete chloroplast genomes in Poaceae. In: Seberg O, Petersen G, Barfod AS, Davis JI (eds) Diversity, phylogeny, and evolution in the monocotyledons. Aarhus University Press, Aarhus, pp 437–450. doi:10.1093/aob/mcr213

    Google Scholar 

  • Edwards EJ, Osborne CP, Strömberg CAE, Smith SA, Bond WJ, Christin P-A, Cousins AB, Duvall MR, Fox DL, Freckleton RP, Ghannoum O, Hartwell J, Huang Y, Janis CM, Keeley JE, Kellogg EA, Knapp AK, Leakey ADB, Nelson DM, Passey BH, Saarela JM, Sage RF, Sala OE, Salamin N, Still CJ, Tipple B (2010) The evolutionary origins of C4 grasslands. Science 328:587–591. doi:10.1126/science.1177216

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. doi:10.1007/BF01734359

    Article  CAS  PubMed  Google Scholar 

  • Givnish TJ, Evans TM, Pires JC, Sytsma KJ (1999) Polyphyly and convergent morphological evolution in Commelinales and Commelinidae: evidence from rbcL sequence data. Mol Phylogenet Evol 12:360–385. doi:10.1006/mpev.1999.0601 1999.0601

    Article  CAS  PubMed  Google Scholar 

  • Givnish TJ, Sevillano M, McNeal J, McKain M, Steele PR, dePamphilis C, Graham S, Pires JC, Stevenson DW, Zomlefer W, Briggs B, Duvall MR, Moore M, Soltis DE, Soltis P, Thiele K, Leebens-Mack J (2010) Assembling the tree of the monocotyledons: plastome sequence phylogeny and evolution of Poales. Ann Mo Bot Gard 97:584–616. doi:10.3417/2010023

    Article  Google Scholar 

  • Grass Phylogeny Working Group I, Barker N, Clark LG, Davis JI, Duvall MR, Guala G, Hsiao C, Kellogg EA, Linder HP, Mason-Gamer R, Mathews SY, Soreng R, Spangler R (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373–457. doi:10.2307/3298585

    Article  Google Scholar 

  • Grass Phylogeny Working Group II, Aliscioni S, Bell H, Besnard G, Christin P-A, Columbus JT, Duvall MR, Edwards EJ, Guissani L, Hasenstab-Lehman K, Hilu K, Hodkinson T, Ingram A, Kellogg EA, Mashayekhi S, Morrone O, Osborne C, Salamin N, Schaefer H, Spriggs E, Smith S, Zuloaga F (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. doi:10.1111/j.1469-8137.2011.03972.x

    Article  CAS  Google Scholar 

  • Graur D, Li W-H (2000) Fundamentals of molecular evolution, 2nd edn. Sinauer, Sunderland

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. doi:10.1080/10635150390235520

    Article  PubMed  Google Scholar 

  • Guo X, Castillo-Ramírez S, González V, Bustos P, Fernández-Vázquez JL, Santamaría RI, Arellano J, Cevallos MA, Dávila G (2007) Rapid evolutionary change of common bean (Phaseolus vulgaris L) plastome, and the genomic diversification of legume chloroplasts. BMC Genom 8:228. doi:10.1186/1471-2164-8-228

    Article  Google Scholar 

  • Handley L, O’ Halloran A, Pearson P, Hawkins E, Nicholas C, Schouten S, McMillan I, Pancost R (2012) Changes in the hydrological cycle in tropical East Africa during the Paleocene–Eocene thermal maximum. Palaeogeogr Palaeoclimatol Palaeoecol 329–330:10–21. doi:10.1016/j.palaeo.2012.02.002

    Article  Google Scholar 

  • Herendeen PS, Crane PR (1995) The fossil history of the monocotyledons. In: Rudall PJ, Cribb P, Cutler DF, Humphries CJ (eds) Monocotyledons: systematics and evolution. Royal Botanic Gardens, Surrey, pp 1–21

    Google Scholar 

  • Igloi G, Meinke A, Dory I, Kossel H (1990) Nucleotide sequence of the maize chloroplast rpoB/C1/C2 operon: comparison between the derived protein primary structures form various organisms with respect to functional domains. Mol Gen Genetics 221:379–394. doi:10.1007/BF00259403

    CAS  Google Scholar 

  • Jacobs BF, Kingston JD, Jacobs LL (1999) The origin of grass-dominated ecosystems. Ann Mo Bot Gard 86:590–643. doi:10.2307/2666186

    Article  Google Scholar 

  • Jaramillo C, Ochoa D, Contreras L, Pagani M, Carvajal-Ortiz H, Pratt LM, Krishnan S, Cardona A, Romero M, Quiroz L, Rodriguez G, Rueda MJ, de la Parra F, Moron S, Green W, Bayona G, Montes C, Quintero O, Ramirez R, Mora G, Schouten S, Bermudez H, Navarrete R, Parra F, Alvaran M, Osorno J, Crowley JL, Valencia V, Vervoort J (2010) Effects of rapid global warming at the Paleocene-Eocene boundary on neotropical vegetation. Science 330:957–961. doi:10.1126/science.1193833

    Article  CAS  PubMed  Google Scholar 

  • Judd W, Campbell C, Kellogg E, Stevens P, Donoghue M (2008) Plant systematics, a phylogenetic approach, 3rd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Judziewicz EJ, Clark LG (2007) Classification and biogeography of New World grasses: Anomochlooideae, Pharoideae, Ehrhartoideae, and Bambusoideae. Aliso 23:303–314

    Article  Google Scholar 

  • Katayama H, Ogihara Y (1993) Structural alteration of the chloroplast genome found in grasses are not common in monocots. Curr Genet 23:160–165

    Google Scholar 

  • Katayama H, Ogihara Y (1996) Phylogenetic affinities of the grasses to other monocots as revealed by molecular analysis of chloroplast DNA. Curr Genet 29:572–581. doi:10.1007/BF02426962

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1093/nar/gki198

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kellogg EA, Campbell CS (1987) Phylogenetic analyses of the Gramineae. In: Soderstrom T, Hilu K, Campbell C, Barkworth M (eds) Grass systematics and evolution. Smithsonian Institution Press, Washington, D. C., pp 310–322

    Google Scholar 

  • 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. doi:10.1007/s00239-009-9275-9

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1006/jmbi.1995.0460

    Article  CAS  PubMed  Google Scholar 

  • Mayer C (2010) Phobos: a tandem repeat search tool for complete genomes, vers. 3.3.11. Ruhr Universität, Bochum, Germany. http://www.rub.de/spezzoo/cm/cm_phobos.htm

  • McLoughlin S (2001) The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Aust J Bot 49:271–300. doi:10.1071/BT00023

    Article  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), New Orleans, LA pp 1–8. doi:10.1109/GCE.2010.5676129

  • 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. doi:10.3732/ajb.0900226

    Article  CAS  PubMed  Google Scholar 

  • Norris R, Röhl U (1999) Carbon cycling and chronology of climate warming during the Palaeocene/Eocene transition. Nature 401:775–778. doi:10.1038/44545

    Article  CAS  Google Scholar 

  • Poinar G, Columbus JT (1992) Adhesive grass spikelet with Mammalian Hair in Dominican Amber: first fossil evidence of epizoochory. Experientiae 48:906–908. doi:10.1007/BF02118433 Vicosa, Braz

    Article  Google Scholar 

  • Prasad V, Strömberg CAE, Alimohammadian H, Sahni A (2005) Dinosaur coprolites and the early evolution of grasses and grazers. Science 310:1177–1180. doi:10.1126/science.1118806

    Article  CAS  PubMed  Google Scholar 

  • Prasad V, Strömberg CAE, Leaché AD, Samant B, Patnaik R, Tang L, Mohabey DM, Ge S, Sahni A (2011) Late Cretaceous origin of the rice tribe provides evidence for early diversification in Poaceae. Nature Comm 2:480. doi:10.1038/ncomms1482

    Article  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2009) TRACER v1.5. http://tree.bio.ed.ac.uk/software/tracer/. Accessed 15 January 2013

  • Sage R (2004) The evolution of C4 photosynthesis. New Phytol 161:341–370. doi:10.1111/j.1469-8137.2004.00974.x

    Article  CAS  Google Scholar 

  • Sajo MG, Longhi-Wagner H, Rudall PJ (2007) Floral development and embryology in the early-divergent grass Pharus. Int J Plant Sci 168:181–191. doi:10.1086/509790 Chicago, IL, USA

    Article  Google Scholar 

  • Sajo MG, Pabón-Mora N, Jardim J, Stevenson DW, Rudall PJ (2012) Homologies of the flower and inflorescence in the early-divergent grass Anomochloa (Poaceae). Am J Bot 99:614–628. doi:10.3732/ajb.1100290

    Article  PubMed  Google Scholar 

  • Schmitz B, Pujalte V (2007) Abrupt increase in seasonal extreme precipitation at the Paleocene-Eocene boundary. Geology 35:215–218. doi:10.1130/G23261A.1

    Article  CAS  Google Scholar 

  • Shimada H, Fukuta M, Ishakawa M, Sugiura M (1990) Rice chloroplast RNA polymerase genes: the absence of an intron in rpoC1 and the presence of an extra sequence in rpoC2. Mol Gen Genet 221:395–402. doi:10.1007/BF00259404

    Article  CAS  PubMed  Google Scholar 

  • Soreng RJ, Davis JI (1998) Phylogenetics and character evolution in the grass family: simultaneous analysis of morphological and chloroplast DNA restriction site character sets. Bot Rev 64:1–85. doi:10.1007/BF02868851

    Article  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 57:758–771. doi:10.1080/10635150802429642

    Article  PubMed  Google Scholar 

  • Strömberg CAE (2005) Decoupled taxonomic radiation and ecological expansion of open-habitat grasses in the Cenozoic of North America. Proc Natl Acad Sci USA 102:11980–11984. doi:10.1073/pnas.0505700102

    Article  PubMed Central  PubMed  Google Scholar 

  • Swofford DL (2003) PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tripati A, Elderfield H (2005) Deep-sea temperature and circulation changes at the Paleocene-Eocene thermal maximum. Science 308:1894–1898. doi:10.1126/science.1109202

    Article  CAS  PubMed  Google Scholar 

  • Tsuji S, Ueda K, Nishiyama T, Hasebe M, Yoshikawa S, Konagaya A, Nishiuchi T, Yamaguchi K (2007) The chloroplast genome from a lycophyte (microphyllophyte), Selaginella uncinata, has a unique inversion, transpositions and many gene losses. J Plant Res 120:281–290. doi:10.1007/s10265-006-0055-y

    Article  CAS  PubMed  Google Scholar 

  • Vicentini A, Barber J, Aliscioni S, Giussani L, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Global Change Biol 14:2963–2977. doi:10.1111/j.1365-2486.2008.01688.x

    Article  Google Scholar 

  • Watson L, Dallwitz M (1992 onwards) The grass genera of the world: descriptions, illustrations, identification, and information retrieval; including synonyms, morphology, anatomy, physiology, phytochemistry, cytology, classification, pathogens, world and local distribution, and references. http://delta-intkey.com. Accessed 17 Jan 2012

  • Weglöhner W, Subramanian AR (1991) A heptapeptide repeat contributes to the unusual length of chloroplast ribosomal protein S18. Nucleotide sequence and map position of the rpl33-rps18 gene cluster in maize. FEBS Lett 279:193–197. doi:10.1016/0014-5793(91)80147-U

    Article  PubMed  Google Scholar 

  • Wu Z-Q, Ge S (2012) The phylogeny of the BEP clade in grasses revisited: evidence from the whole genome sequences of chloroplasts. Mol Phylogenet Evol 62:573–578. doi:10.1016/j.ympev.2011.10.019

    Article  PubMed  Google Scholar 

  • Wu F-H, Kan D-P, Lee S-B, Daniell H, Lee Y-W, Lin C–C, Lin N-S, Lin C-S (2009) Complete nucleotide sequence of Dendrocalamus latiflorus and Bambusa oldhamii chloroplast genomes. Tree Physiol 29:847–856. doi:10.1093/treephys/tpp015

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phylogenet Evol 26:1–7

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y-J, Ma P-F, Li D-Z (2011) High-throughput sequencing of six bamboo chloroplast genomes: phylogenetic implications for temperate woody bamboos (Poaceae: Bambusoideae). PLoS One 6:1–16. doi:10.1371/journal.pone.0020596

    Google Scholar 

Download references

Acknowledgments

We thank J. Triplett, Jacksonville State University, Alabama, for fresh specimens and the Missouri Botanical Garden for dried specimens. We also thank J. Chris Pires, Patrick Edger, and Dustin Mayfield for technical assistance. We thank three anonymous reviewers whose comments improved the paper. This work was supported in part by the Plant Molecular Biology Center and the Department of Biological Sciences at Northern Illinois University as well as by the National Science Foundation under Grant Number (DEB-1120761) to MRD. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Melvin R. Duvall.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, S.S., Burke, S.V. & Duvall, M.R. Phylogenomics, molecular evolution, and estimated ages of lineages from the deep phylogeny of Poaceae. Plant Syst Evol 300, 1421–1436 (2014). https://doi.org/10.1007/s00606-013-0971-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-013-0971-y

Keywords

Navigation