Skip to main content
SpringerLink
Log in

Phylogenetic analysis of Lappula Moench (Boraginaceae) based on molecular and morphological data

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

Abstract

Lappula Moench includes ca. 70 species and exhibits a wide range of nutlet variation. Currently, the evolutionary relationships among species of Lappula have not been examined; therefore, to elucidate phylogenetic relationships and morphological evolution within Lappula and related genera, we conducted phylogenetic analyses with matrices that include 48 species as well as four DNA regions (ITS, trnL-trnF, rpS16 and psbA-trnH) and 18 morphological characters. These matrices were analyzed using maximum parsimony, maximum likelihood, and Bayesian inference methods. Analyses of the combined molecular and morphological data result in a phylogeny that is better resolved than that based solely on molecular sequence data. Phylogenetic results suggest that the current infrageneric classification of Lappula, at least at the subsectional and series level, is artificial. The evolutionary patterns of 18 morphological characters are investigated in a phylogenetic context. In Lappula, nutlet homomorphism and small corollas are resolved as ancestral, while nutlet heteromorphism and larger corollas are derived.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Al-Shehbaz I (1991) The genera of Boraginaceae in the southeastern United States. J Arnold Arbor Suppl Ser 1:1–169

    Google Scholar 

  • Baillon H (1888) Boraginacées. In: Baillon H. Hist. Pl. Librairie Hachette and Cie, Paris, pp 343–402

  • Bentham G, Hooker JD (1873) Genera Plantarum, vol 2. Lovell Reeve and Co, Williams and Norgate, London

    Google Scholar 

  • Brand A (1931) Boraginaceae-Boraginoideae-Cryptantheae. In: Engler A. Das Pflanzenreich, vol 4. Leipzig, pp 236

  • Carr RL (1973) A taxonomic study in the genus Hackelia in western North America. Oregon State University

  • Chater AO (1972) Lappula. Gilib. In: Tutin TG, Heywood VH, Burges NA (eds) Flora Europaea, vol 3. Diapensiaceae to Myoporaceae. Cambridge University Press, London, pp 117–118

  • Chu GL, Kamelin R (1995) Nomenclatural notes on the Boraginaceae of China. Novon 5:17–18

    Article  CAS  Google Scholar 

  • Cronquist A, Holmgren AH, Holmgren NH, Reveal JL, Holmgren PK (1984) Intermountain flora: vascular plants of the intermountain west, USA vol 4. subclass Asteridae (except Asteraceae). New York Botanical Garden, New York

  • de Candolle A (1845) Prodromus Systematis naturalis regni vegetabilis, Paris

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416

    Article  Google Scholar 

  • Frick B (1984) The biology of Canadian weeds: 62. Lappula squarrosa (Retz.) Dumort. Can J Plant Sci 64:375–386

    Article  Google Scholar 

  • Gilibert JE (1782) Flora Lituanica. Grodnae, pp 66

  • Gürke M (1897) Boraginaceae. In: Engler A, Prantl K. Die natürlichen Pflanzenfamilien Engelmann, vol 4. Leipzig, pp 71–131

  • Hasenstab KE (2009) Molecular phylogenetic systematics of the plant genus Cryptantha (Boraginaceae). San Diego State University

  • Higgins LC (1972) The Boraginaceae of Utah. Brigham Young University Science Bull. Biological series vol 16:54–60

    Google Scholar 

  • Higgins LC (1979) Boraginaceae of the southwestern united states. West N Am Naturalist 39:293–350

    Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Bio 42:182–192

    Google Scholar 

  • Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hultén E (1971) The circumpolar plants. II. Dicotyledons. Almqvist and Wikselt, Stockholm, p 463

    Google Scholar 

  • Johnston IM (1923) Studies in the Boraginaceae, I. Contributions from the Gray Herbarium, Harvard University, 68:43–80

  • Kang Y, Zhang ML, Chen ZD (2003) A preliminary phylogenetic study of the subgenus Pogonophace (Astragalus) in China based on ITS sequence data. Acta Bot Sin 45:140–145

    CAS  Google Scholar 

  • Khoshsokhan M, Osaloo SK, Saadatmand S, Attar F (2010) Molecular phylogeny of Rochelia (Broaginaceae) based on nrDNA ITS and cpDNA trnL-F sequences. Iran J Bot 16:22–29

    Google Scholar 

  • Långström E, Chase M (2002) Tribes of Boraginoideae (Boraginaceae) and placement of Antiphytum, Echiochilon, Ogastemma and Sericostoma: a phylogenetic analysis based on atpB plastid DNA sequence data. Plant Syst Evol 234:137–153

    Article  Google Scholar 

  • Lehmann JGC (1818) Plantae e familia Asperifoliarum nuciferae. Dümmler, Berlin, p 78

    Google Scholar 

  • Lian YS, Wang JQ (1990) Eritrichium Schrad In: Kung XW, Wang WC. Flora Reipublicae Popularis Sinicae, vol. 62 (in Chinese). Science Press, Beijing, pp 116–150

  • Ma WB, Zhao XJ, Tan DY, Baskin CC, Baskin JM, Xue JH (2010) Nutlet dimorphism in individual flowers of two cold desert annual Lappula species (Boraginaceae): implications for escape by offspring in time and space. Plant Ecol 209:361–374

    Article  Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade, version 3.0: analysis of phylogeny and character evolution. Sunderland: Sinauer Associates

  • Mao ZM, Zhang DM (1994) The conspectus of ephemeral flora in northern Xinjiang (in Chinese with English abstract). Arid Zone Res 11:1–26

    CAS  Google Scholar 

  • McEvoy PB (1984) Dormancy and dispersal in dimorphic achenes of tansy ragwort, Senecio jacobaea L. (Compositae). Oecologia 61:160–168

    Article  Google Scholar 

  • Mozaffar MK, Osaloo SK, Oskoueiyan R, Saffar KN, Amirahmadi A (2013) Tribe Eritrichieae (Boraginaceae s.str.) in West Asia: a molecualr phylogenetic perspective. Plant Syst Evol 299:197–208

    Article  Google Scholar 

  • Nasir YJ (1989) In Nasir YJ, Ali SI. Flora of Pakistan, vol 191, pp 137-149

  • Nazaire M, Hufford L (2012) A broad phylogenetic analysis of Boraginaceae: implications for the relationships of Mertensia. Syst Bot 37:758–783

    Article  Google Scholar 

  • Nelson A (1899) New Plants from Wyoming. VII. Bull Torrey Bot Club 26:236–250

    Article  Google Scholar 

  • Nelson A, MacBride JF (1916) Western plant studies. III. Bot Gaz 61:30–47

    Article  Google Scholar 

  • Ovchinnikova SV (2005) The system of the subtribe Echinosperminae (Boraginaceae) (in Russian with English abstract). Bot Zhurn 90:1153–1172

    Google Scholar 

  • Ovchinnikova SV (2006) Ultrasculptural features of fruit surface in subtribe Echinosperminae (tribe Eritrichieae, Boraginaceae) (in Russian with English abstract). Bot Zhurn 91:105–116

    Google Scholar 

  • Ovchinnikova SV (2009) On the position of the tribe Eritrichieae in the Boraginaceae system. Bot Serbica 33:141–146

    Google Scholar 

  • Oxelman B, Lidén M, Berglund D (1997) Chloroplast rpS16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Syst Evol 206:393–410

    Article  Google Scholar 

  • Popov MG (1953) Boraginaceae. In: Shishkin B K. Flora U.S.S.R. vol 19. Moskwa and Leningrad, pp 97–691

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Riedl H (1967) Lappula Gilib. in Rechinger KH. Flora Iranica, vol 48. Akademisch Druck u. Verlagsanstalt, Graz, pp 68–84

  • Riedl H (1997) Boraginaceae. In: Kalkman C, Noteboom HP, de Wilde WJ (eds) Flora Malesiana, Series 1, Spermatophyta Publications Department, Rijksherbarium, Leiden, pp 13:43–168

  • Sadat F (1989) Revision ausgewählter kritischer Gattungen der Boraginaceen aus der Flora Afghanistans. - Mitt. Bot. Staatssammlung München 28:1–210

    Google Scholar 

  • Sang T, Crawford DJ, Stuessy TF (1997) Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am J Bot 84:1120–1136

    Article  PubMed  CAS  Google Scholar 

  • Stevens OA (1922) New records and other notes on North Dakota plants. Bull Torrey Bot Club 49:93–105

    Article  Google Scholar 

  • Sun YX, Zhang ML (2012) Molecular phylogeny of tribe Atraphaxideae (Poly-gonaceae) evidenced from five cpDNA genes. J Arid Land 4:180–190

    Article  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and other method), version 4.0. Sunderland: Sinauer Associates

  • Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109

    Article  PubMed  CAS  Google Scholar 

  • Takhtajan AL (1997) Diversity and classification of flowering plants. Columbia University Press, New York

    Google Scholar 

  • Tate JA, Simpson BB (2003) Paraphyly of Tarasa (Malvaceae) and diverse origins of the polyploid species. Syst Bot 28:723–737

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Venable DL (1985) The evolutionary ecology of seed heteromorphism. Am Nat 126:577–595

    Article  Google Scholar 

  • Wang CJ (1981) A study on the genus Lappula of China (in Chinese with English abstract). Bull Bot Res 1:77–100

    Google Scholar 

  • Wang WT (1984) Notulae de Boraginaceis sinensibus (in Chinese with English abstract). Bull Bot Res 4:1–13

    Google Scholar 

  • Wang QR (1990) Lappula V. Wolf. In: Kung XW, Wang WC. Flora Reipublicae Popularis Sinicae, vol 62. (in Chinese). Science Press, Beijing, pp 177–207

  • Wang ZJ, Pi XM (1997) New taxa of Lappula V. Wolf. From Xinjiang (in Chinese). J Xinjiang Univ 14:66–68

    CAS  Google Scholar 

  • Weigend M, Gottschling M, Selvi F, Hilger HH (2010) Fossil and extant Western Hemisphere Boragineae, and the polyphyly of “Trigonotideae” Riedl (Boraginaceae: Boraginoideae). Syst Bot 35:409–419

    Article  Google Scholar 

  • White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: A guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Willson MF (1983) Plant reproductive ecology. Wiley, New York

    Google Scholar 

  • Wu ZY, Wang H (1983) Plany geography (in Chinese). Science Press, Beijing, pp 62–63

    Google Scholar 

  • Xue JJ, Zhang ML (2011) Monophyly and infrageneric variation of Corispermum L. (Chenopodiaceae), evidence from sequence data psbB-psbH, rbcL and ITS. J Arid Land 3:240–253

    Article  Google Scholar 

  • Zhu GL, Riedl H, Kamelin RV (1995) Boraginaceae. In: Wu ZY, Raven PH (eds) Flora of China, vol 16. Science Press, Beijing, pp 329–427

    Google Scholar 

Download references

Acknowledgments

This research was funded by the CAS Important Direction for Knowledge Innovation Project (KZCX2-EW-305), and Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences. Thanks to Prof. AnRen LI (Institute of Botany, CAS, China) for his helpful identification to our field samples, to Dr. Stewart C. Sanderson (Shrub Sciences Laboratory, USDA, Utah, USA) for his offering of the American Lappula materials. Thanks specially to anonymous reviewers for their valuable and constructive suggestions.

Author information

Authors and Affiliations

  1. Key Laboratory of Biogeography and Bioresource in Arid Land, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, 830011, China

    Jian-Feng Huang & Ming-Li Zhang

  2. Graduate University, Chinese Academy of Sciences, Beijing, 100049, China

    Jian-Feng Huang

  3. Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Ming-Li Zhang

  4. Department of Biology and Chemistry, Texas A&M International University, Laredo, TX, 78041, USA

    James I. Cohen

Authors
  1. Jian-Feng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming-Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James I. Cohen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ming-Li Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, JF., Zhang, ML. & Cohen, J.I. Phylogenetic analysis of Lappula Moench (Boraginaceae) based on molecular and morphological data. Plant Syst Evol 299, 913–926 (2013). https://doi.org/10.1007/s00606-013-0772-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-013-0772-3

Keywords

Search

Navigation