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1 July 2009 The petD group II intron as a species level marker: utility for tree inference and species identification in the diverse genus Campanula (Campanulaceae)
Thomas Borsch, Nadja Korotkova, Thomas Raus, Wolfram Lobin, Cornelia Löhne
Author Affiliations +
Abstract

Borsch T., Korotkova N., Raus T., Lobin W. & Löhne C.: The petD group II intron as a species level marker: utility for tree inference and species identification in the diverse genus Campanula (Campanulaceae). — Willdenowia 39: 7–33. — Online ISSN 1868-6397; © 2009 BGBM Berlin-Dahlem. doi:10.3372/wi.39.39101 (available via  http://dx.doi.org/)

Chloroplast introns have a high potential as tools for phylogeny inference and DNA barcoding. This study examines the molecular evolution of the petD group II intron in Campanulaceae based on a sequence data set of 114 ingroup taxa. Three small mutational hotspots had to be excluded from phylogenetic analysis, the two most variable being located in the D4 loop (domain IV). A (GT)4–7 microsatellite in domain II is conserved at species level but of limited phylogenetic use due to unclear homology of individual repeat units. Sequences of the petD group II intron depict Cyphioideae, Lobelioideae and Campanuloideae as major Campanulaceae clades. Core Campanuloideae comprise two major radiations of Campanula species: a Musschia clade (including C. lactiflora) and a Jasione clade. Campanula is highly paraphyletic to a number of smaller genera such as Azorina, Michauxia and Edraianthus. The closed-tubular flowered taxa (Phyteuma and allies) are resolved sister to C. persicifolia. Within core campanuloids petD sequences identify 90 % of the taxon samples included in this study. Considering the ease of amplification and sequencing, and its high information content, the petD intron appears to be a good candidate in a two-tailed approach integrating molecular phylogenetics and species identification in the needed sampling of all core Campanuloideae species.

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References

1.

D. C. Albach , P. S. Soltis , D. E. Soltis & R.G. Olmstead 2001: Phylogenetic analysis of asterids based on sequences of four genes. — Ann. Missouri Bot. Gard. 88: 163–212. [  CrossRefGoogle Scholar

2.

A. Antonelli 2008: Higher level phylogeny and evolutionary trends in Campanulaceae subfam. Lobelioideae: molecular signal overshadows morphology. — Mol. Phylogenet. Evol. 46: 1–18. [  CrossRefGoogle Scholar

3.

APG II 2003: An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants. — Bot. J. Linn. Soc. 141: 399–436. [  CrossRefGoogle Scholar

4.

M. H. J. Barfuss , R. Samuel , W. Till & T. F Stuessy 2002: Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions. — Amer. J. Bot. 92: 337–351. [  CrossRefGoogle Scholar

5.

M. H. J. Barfuss , R. Samuel , W. Till & T. F Stuessy 2005: Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions. — Amer. J. Bot. 92: 337–351. [  CrossRefGoogle Scholar

6.

A. A. Belyaev 1984a: Anatomiya semyan nekotorykh predstanitelei semeistva Campanulaceae [Seed anatomy in some representatives of the family Campanulaceae]. — Bot. Zhurn. (Moscow & Leningrad) 69: 585–594. Google Scholar

7.

A. A. Belyaev 1984b: Ul'trastruktura poverkhnosti i nekotorye morphologicheskie kharakteristiki semyan predstanitelei semeistva Campanulaceae [Surface ultrastructure and some morphological characteristics of seeds in the representatives of the family Campanulaceae]. — Bot. Zhurn. (Moscow & Leningrad) 69: 890–898. Google Scholar

8.

T. Borsch & D. Quandt 2009: Mutational dynamics and phylogenetic utility of non-coding chloroplast DNA. — Pl Syst. Evol. [  CrossRefGoogle Scholar

9.

T. Borsch , K. W. Hilu , D. Quandt , V. Wilde , C. Neinhuis & W. Barthlott 2003: Non-coding plastid trnT-trnF sequences reveal a well resolved phylogeny of basal angiosperms. — J. Evol. Biol. 16: 558–576. [  CrossRefGoogle Scholar

10.

B. Bremer , K. Bremer , N. Heidari , P. Erixon , R. G. Olmstead , A. A. Anderberg , M. Kallersjo & E. Barkhordarian 2002: Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels. — Mol. Phylogenet. Evol. 24: 274–301. [  CrossRefGoogle Scholar

11.

K. P. Buttler 2002: Beitrag zu Kenntnis von Campanula baumgartenii. — Bot. Natursch. Hessen 14: 77–90. Google Scholar

12.

A. L. P. P. de Candolle 1830: Monographie des Campanulees. — Paris. Google Scholar

13.

J. Cano-Maqueda , S. Talavera , M. Arista & P. Catalán 2008: Speciation and biogeographical history of the Campanula lusitanica complex (Campanulaceae) in the Western Mediterranean region. — Taxon 57: 1252–1266. Google Scholar

14.

A. Carlström 1986: A revision of the Campanula drabifolia complex (Campanulaceae). — Willdenowia 15: 375–387. Google Scholar

15.

N. Cellinese , S. A. Smith , E. J. Edwards , S.-T. Kim , R. C. Haberle , M. Avramakis & M. J. Donoghue 2009: Historical biogeography of the endemic Campanulaceae of Crete. — J. Biogeogr. [  CrossRefGoogle Scholar

16.

F. Conti , G. Abbate , A. Alessandrini & C. Blasi (ed.) 2005: An annotated checklist of the Italian vascular flora. — Roma. Google Scholar

17.

A. Cronquist 1988: The evolution and classification of flowering plants. — New York. Google Scholar

18.

J. Damboldt 1965: Zytotaxonomische Revision der isophyllen Campanulae in Europa. — Bot. Jahrb. Syst. 84: 302–358. Google Scholar

19.

J. Damboldt 1976: Phyteuma L. — Pp. 95–98 in: T. G. Tutin , V. H. Heywood , N. A. Burges , D. M. Moore , D. H. Valentine , S. M. Walters & D. A. Webb (ed.), Flora europaea 4. — Cambridge, etc. Google Scholar

20.

J. Damboldt 1978: Campanula L. — Pp. 2–64 in: P. H. Davis (ed.), Flora of Turkey and the East Aegean Islands. — Edinburgh. Google Scholar

21.

D. S. Devey , M. W. Chase & J. J. Clarkson 2009: A stuttering start to plant DNA barcoding: microsatellites present a previously overlooked problem in noncoding plastid regions. — Taxon 58: 7–15. Google Scholar

22.

A. Dunbar 1975a: On pollen of Campanulaceae and related families with special reference to surface ultrastructure. I. Campanulaceae subfam. Campanuloideae. — Bot. Not. 128: 73–101. Google Scholar

23.

A. Dunbar 1975b: On pollen of Campanulaceae and related families with special reference to surface ultrastructure. I. Campanulaceae subfam. Cyphioideae and subfam. Lobelioideae; Goodeniaceae; Sphenocleaceae. — Bot. Not. 128: 102–118. Google Scholar

24.

W. M. M. Eddie , T. Shulkina , J. Gaskin , R. C. Haberle & R. K. Jansen 2003: Phylogeny of Campanulaceae s.str. inferred from ITS sequences of nuclear ribosomal DNA. — Ann. Missouri Bot. Gard. 90: 554– 575. [  CrossRefGoogle Scholar

25.

F. Ehrendorfer , J.-F. Manen & A. Natali 1994: cpDNA intergene sequences corroborate restriction site data for reconstructing Rubiaceae phylogeny. — Pl. Syst. Evol. 190: 245–248. [  CrossRefGoogle Scholar

26.

A. A. Fedorov 1957: Campanulaceae. — Pp. 459–475 in: B. K. Shishkin (ed.), Flora SSSR 24. — Moscow. Google Scholar

27.

A. A. Fedorov & M. Kovanda 1976: Campanula. — Pp. 74–93 in: T. G. Tutin , V. H. Heywood , N. A. Burges , D. M. Moore , D. H. Valentine , S. M. Walters & D. A. Webb (ed.), Flora europaea 4. — Cambridge, etc. Google Scholar

28.

J. Fielding , N. Turland & B. Mathew 2005: Flowers of Crete. — Kew. Google Scholar

29.

R. Gagnidze 2005: Vascular plants of Georgia. A nomenclatural checklist. — Tbilisi. Google Scholar

30.

W. Greuter , H. M. Burdet & G. Long 1984: Med-Checklist 1. — Genève & Berlin. Google Scholar

31.

I. Groeninckx , P. de Block , F. Rakotonasolo , E. Smets & S. Dessein 2009: Rediscovery of Malagasy Lathraeocarpa allows determination of its taxonomic position within Rubiaceae. — Taxon 58: 209–226. Google Scholar

32.

M. B. Hamilton 1999: Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. — Molec. Ecol. 8: 521–523. Google Scholar

33.

A. Hayek 1928–31 : Prodromus florae peninsulae balcanicae 2 [pp. 1–96 (1928), pp. 97–336 (1929), pp. 337–576 (1930), pp. 577–1152 (1931)]. — Repert. Spec. Nov. Regni Veg. Beih. 30(2). Google Scholar

34.

J. P. Huelsenbeck & F. Ronquist 2001: MRBAYES: Bayesian inference of phylogenetic trees. — Bioinformatics 17: 754–755. [  CrossRefGoogle Scholar

35.

R. W. Jobson , J. Playford , K. M. Cameron & V. A. Albert 2003: Molecular phylogenetics of Lentibulariaceae inferred from plastid rps 16 intron and trnL-F DNA sequences: implications for character evolution and biogeography. — Syst. Bot. 28: 157–171. Google Scholar

36.

J. Kårehed , I. Groeninckx , S. Dessein , T. J. Motley & B. Bremer 2008: The phylogenetic utility of chloroplast and nuclear DNA markers and the phylogeny of Rubiaceae tribe Spermacoceae. — Molec. Phylogenet. Evol. 49: 843–866. [  CrossRefGoogle Scholar

37.

S. A. Kelchner 2002: Group II introns as phylogenetic tools: structure, function, and evolutionary constraints. — Amer. J. Bot. 89: 1651–1669. [  CrossRefGoogle Scholar

38.

A. Kocyan , L.-B. Zhang , H. Schaefer & S. S. Renner 2007: A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. — Mol. Phylogenet. Evol. 44: 553–577. [  CrossRefGoogle Scholar

39.

A. A. Kolakovsky 1987: Systema semeistva Campanulaceae starogo sveta [System of the Campanulaceae family from the Old World]. — Bot. Zhurn. (Moscow & Leningrad) 72: 1572–1579. Google Scholar

40.

A. A. Kolakovsky 1992: Campanulaceae. — Pp. 170–171 in: H. Meusel & E. J. Jäger (ed.), Vergleichende Chorologie der zentraleuropäischen Flora 3. – Jena, etc. Google Scholar

41.

A. A. Kolakovsky 1994: Konspekt sistemy semeistva Campanulaceae starogo sveta [The conspectus of the system of Old World Campanulaceae]. — Bot. Zhurn. (Moscow & Leningrad) 79(1): 109–124. Google Scholar

42.

N. Korotkova , J. V. Schneider , D. Quandt , A. Worberg , G. Zizka & T. Borsch 2009: Phylogeny of the eudicot order Malpighiales: analysis of a recalcitrant clade with sequences of the petD group II intron. — Pl. Syst. Evol. [  CrossRefGoogle Scholar

43.

M. Kovanda 1970a: Polyploidy and variation in the Campanula rotundifolia complex. Part 1 (General). — Rozpr. Českoslov. Akad. Ved. 80: 1–95. Google Scholar

44.

M. Kovanda 1970b: Polyploidy and variation in the Campanula rotundifolia complex. Part 2 (Taxonomy). 1. Revision of the groups Saxicolae, Lanceolatae and Alpicolae in Czechoslovakia and adjacent regions. — Folia Geobot. Phytotax. 5: 171–208. Google Scholar

45.

M. Kovanda 1977: Polyploidy and variation in the Campanula rotundifolia complex. Part 2 (Taxonomy). 1. Revision of the groups Vulgares and Scheuchzerianae in Czechoslovakia and adjacent regions. — Folia Geobot. Phytotax. 12: 23–89. Google Scholar

46.

S. Kovačić 2004: The genus Campanula L. (Campanulaceae) in Croatia, circum-Adriatic and West Balkan region. — Acta Bot. Croat. 63: 171–202. Google Scholar

47.

D. Lakušić 1974: Prirodni system populacija I vrsta roda Edraianthus DC. — God. Biol. Inst. Univ. Sarajevu 26: 1–30. Google Scholar

48.

D. Lakusic & F. Conti 2004: Asyneuma pichleri (Campanulaceae), a neglected species of the Balkan Peninsula. — Pl. Syst. Evol. 247: 23–36. Google Scholar

49.

T. G. Lammers 2007: Campanulaceae. – Pp. 36—56 in: J. W. Kadereit & Jeffrey (volume ed.), Families and genera of vascular plants 8. — Berlin, etc. Google Scholar

50.

M. Łańcucka-Środoniowa 1977: New herbs described from the Tertiary of Poland. — Acta Palaeobot. 18: 37–42. Google Scholar

51.

M. Łańcucka-Srodoniowa 1979: Macroscopic plant remains from the freshwater Miocene of the Nowy Sacz basin (West Carpathians, Poland). — Acta Palaeobot. 20: 74–75. Google Scholar

52.

K. Lehmann & U. Schmidt 2003: Group II introns: structure and catalytic versatility of large natural ribozymes. — Crit. Rev. Biochem. Molec. Biol. 38: 249–303. [  CrossRefGoogle Scholar

53.

C. Löhne & T. Borsch 2005: Molecular evolution and phylogenetic utility of the petD group II intron: a case study in basal angiosperms. — Molec. Biol. Evol. 22: 317–332. [  CrossRefGoogle Scholar

54.

C. Löhne , T. Borsch & J. H. Wiersema 2007: Phylogenetic analysis of Nymphaeales using fast-evolving and non-coding chloroplast markers. — Bot. J. Linn. Soc. 154: 141–163. [  CrossRefGoogle Scholar

55.

J. Lundberg & K. Bremer 2003: A phylogenetic study of the order Asterales using one morphological and three molecular data sets. — Int. J. Pl. Sci. 164: 553– 578. [  CrossRefGoogle Scholar

56.

J. F. Manen , A. Natali & F. Ehrendorfer 1994a: Phylogeny of Rubiaceae-Rubieae inferred from the sequence of a cpDNA intergene region. — Pl. Syst. Evol. 190: 195–211. [  CrossRefGoogle Scholar

57.

D. H. Mathews , J. S. Schröder , D. H. Turner & M. Zuker 2006: Predicting RNA secondary structure. — Pp. 631–657 in: R. F. Oesteland , T. R. Cech & J. F. Atkins (ed.), The RNA world, ed. 3. — Cold Spring Harbor. Google Scholar

58.

D. H. Mathews , M. D. Disney , J. L. Childs , S. J. Schroeder , M. Zuker & D. H. Turner 2004: Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. — Proc. Natl. Acad. Sci. USA 101: 7287–7292. [  CrossRefGoogle Scholar

59.

F. Michel , K. Umesono & H. Ozeki 1989: Comparative and functional anatomy of group II catalytic introns: a review. — Gene 82: 5–30. [  CrossRefGoogle Scholar

60.

J. Müller , K. Müller , C. Neinhuis & D. Quandt 2005+: PhyDE: Phylogenetic Data Editor. —  www.phyde.de  Google Scholar

61.

K. Müller 2004a: PRAP — computation of Bremer support for large datasets. — Mol. Phylogenet. Evol. 31: 780–782. [  CrossRefGoogle Scholar

62.

K. Müller 2004b: GRate: relative rate test for groups of taxa using general DNA substitution models in PAUP. —  http://systevol.nees.uni-bonn.de/software/ GRate  Google Scholar

63.

K. Müller 2005a: SeqState: Primer design and sequence statistics for phylogenetic DNA datasets. — Appl. Bioinformatics 4: 65–69. Google Scholar

64.

K. Müller 2005b: The efficiency of different search strategies in estimating parsimony jackknife, bootstrap, and Bremer support. — BMC Evol. Biol. 5: no. 58. [  CrossRefGoogle Scholar

65.

K. Müller , T. Borsch & K. W. Hilu 2006: Phylogenetic utility of rapidly evolving DNA at high taxonomical levels: contrasting matK, trnT-F and rbcL in basal angiosperms. — Mol. Phylogenet. Evol. 41: 99–117. [  CrossRefGoogle Scholar

66.

K. Müller , T. Borsch , L. Legendre , S. Porembski , I. Theisen & W. Barthlott 2004: Evolution of carnivory in Lentibulariaceae and the Lamiales. — Pl. Biol. 6: 477–490. [  CrossRefGoogle Scholar

67.

J.-M. Park , S. Kovačić , Z. Liber , W. M. M. Eddie & G. M. Schneeweiss 2006: Phylogeny and biogeography of isophyllous species of Campanula (Campanulaceae) in the Mediterranean area. — Syst. Bot. 31: 862–880. [  CrossRefGoogle Scholar

68.

D. Phitos 1964: Trilokuläre Campanula-Arten der Ägäis. — Österr. Bot. Z. 111: 208–230. [  CrossRefGoogle Scholar

69.

D. Phitos 1965: Die quinquelokulären Camp anula-Arten. — Österr. Bot. Z. 112: 449–498. [  CrossRefGoogle Scholar

70.

D. Podlech 1965: Revision der europäischen und nord-afrikanischen Vertreter der Subsect. Heterophylla (Wit.) Fed. der Gattung Campanula L. — Feddes Repert. 71: 50–187 Google Scholar

71.

D. Podlech 2008: Campanulaceae. — Pp. 182–322 in: G. Wagenitz (volume ed.), Gustav Hegi Illustrierte Flora von Mitteleuropa, ed. 2, 6(2A). — Jena. Google Scholar

72.

D. Podlech & J. Damboldt 1964: Zytotaxonomische Beiträge zur Kenntnis der Campanulaceen in Europa. — Ber. Deutsch. Bot. Ges. 76: 360–369. Google Scholar

73.

D. Posada & K. A. Crandall 1998: Modeltest: testing the model of DNA substitution. — Bioinformatics 14: 817–818. [  CrossRefGoogle Scholar

74.

Y.-L. Qiu , J. Lee , F. Bernasconi-Quandroni , D. E. Soltis , P. S. Soltis , M. Zanis , E. A. Zimmer , Z. Chen , V. Savolainen & M. W. Chase 1999: The earlierst angiosperms: evidence from mitochondrial, plastid and nuclear genomes. — Nature 402: 404–407. [  CrossRefGoogle Scholar

75.

Y.-L. Qiu , O. Dombrovska , J. Lee , L. Li , B. A. Whitlock , F. Bernasconi-Quadroni , J. S. Rest , T. Borsch , K. W. Hilu , S. Renner , D. E. Soltis , P. S. Soltis , M. J. Zanis , J.C. Gutell , M. Powell , V. Savolainen , L. W. Chatrou & M. W. Chase 2005: Phylogenetic analyses of basal angiosperms based on nine plastid, mitochondrial, and nuclear genes. — Int. J. Pl. Sci. 166: 815–842. [  CrossRefGoogle Scholar

76.

D. Quandt & M. Stech 2003: Molecular systematics of bryophytes in context of land plant evolution. — Pp. 267–295 in: A. K. Sharma & A. Sharma (ed.), Plant genome: biodiversity and evolution 1. — Enfield. Google Scholar

77.

D. L. Rabosky 2006: Likelihood methods for detecting temporal shifts in diversification rates. — Evolution 60: 1152–1164. Google Scholar

78.

S. S. Renner 2005: Relaxed molecular clocks for dating historical plant dispersal events. — Trends Pl Sci. 10: 550–558. [  CrossRefGoogle Scholar

79.

P. de Rijk , J. Wuyts & R. D. Wachter 2003: RnaViz2: an improved representation of RNA secondary structure. — Bioinformatics 19: 299–300. [  CrossRefGoogle Scholar

80.

C. Roquet , L. Sáez , J. J. Aldasoro , A. Susanna , M. L. Alcarón & N. Garcia-Jacas 2008: Natural delineation, molecular phylogeny and floral evolution in Campanula. — Syst. Bot. 33: 203–217. [  CrossRefGoogle Scholar

81.

M. J. Sanderson 2002: Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. — Molec. Biol. Evol. 19: 101– 109. Google Scholar

82.

T. Sang , D. Crawford & T. F. Stuessy 1997: Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). — Amer. J. Bot. 84: 1120–1136. [  CrossRefGoogle Scholar

83.

V. Savolainen , M. F. Fay , D. C. Albach , M. Backlund , M. Van der Bank , C. M. Cameron , S. A. Johnson , L. Lledo , J. C. Pintaud , M. Powell , M. C. Sheanan , D. E. Soltis , P. S. Soltis , P. Weston , W. M. Whitten , K. J. Wurdack & M. W. Chase 2000: Phylogeny of the eudicots: a nearly complete familial analysis of the rbcL gene sequences. — Kew Bull. 55: 257–309. [  CrossRefGoogle Scholar

84.

S. Schönland 1889: Campanulaceae. — Pp. 40–70 in: A. Engler & K. Prantl (ed.), Die natürlichen Pflanzenfamilien 4(5). — Leipzig. Google Scholar

85.

J. Shaw , E. B. Lickey , E. E. Schilling & R. L. Small 2007: Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. — Amer. J. Bot. 94: 275–288. [  CrossRefGoogle Scholar

86.

T. V. Shulkina 1979: K voprosu o sistematicheskom polozhenii Campanula lactiflora Bieb. [De positione systematica Campanula lactiflora Bieb.]. — Novosti Sist. Vyssh. Rast. 16: 175–179. Google Scholar

87.

T. V. Shulkina , J. F. Gaskin & W. M. M. Eddie 2003: Morphological studies toward an improved classification of Campanulaceae s.str. — Ann. Missouri Bot. Gard. 90: 576–591. [  CrossRefGoogle Scholar

88.

M. P. Simmons & H. Ochoterena 2000: Gaps as characters in sequence-based phylogenetic analyses. — Syst. Biol. 49: 369–381. [  CrossRefGoogle Scholar

89.

R. L. Small , J. A. Ryborn , R. C. Cronn , T. Seelanan & J. F. Wendel 1998: The tortoise and the hare: choosing between noncoding plastome and nuclear Adh sequences for phylogenetic reconstruction in a recently diverged plant group. — Amer. J. Bot. 85: 1301–1315. [  CrossRefGoogle Scholar

90.

S. A. Smith & M. J. Donoghue 2008: Rates of molecular evolution are linked to life history in flowering plants. — Science 322: 86–89. [  CrossRefGoogle Scholar

91.

D. E. Soltis , P. S. Soltis , M. W. Chase , M. E. Mort , D. C. Albach , M. Zanis , V. Savolainen , W. H. Hahn , S. B. Hoot , M. F. Fay , M. Axteil , S. M. Swensen , L. M. Prince , J. W. Kress , K. C. Nixon & J. S. Farris 2000: Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences. — Bot. J. Linn. Soc. 133: 381–461. [  CrossRefGoogle Scholar

92.

S. Stefanović , D. Lakušić , M. Kuzmina , S. Medeović , K. Tan & V. Stefanović 2008: Molecular phylogeny of Edraianthus (Grassy Bells; Campanulaceae) based on non-coding plastid DNA sequences. — Taxon 57: 452–475. Google Scholar

93.

A. Strid & K. Tan (ed.) 1991: Mountain flora of Greece 2. — Edinburgh. Google Scholar

94.

D. L. Swofford 1998: PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods). — Sunderland. Google Scholar

95.

P. Taberlet , L. Gielly , G. Pautou & J. Bouvet 1991: Universal primers for amplification of 3 noncoding regions of chloroplast DNA. — Pl. Molec. Biol. 17: 1105–1109. [  CrossRefGoogle Scholar

96.

P. Taberlet , E. Coissac , F. Pompanon , L. Gielly , C. Miquel , A. Valentini , T. Vermat , G. Corthier , C. Brochmann & E Willerslev 2007: Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. — Nucl. Acids Res. 35: e14 [  CrossRefGoogle Scholar

97.

A. Takhtajan 1997: Diversity and classification of flowering plants. — New York. Google Scholar

98.

K. Tan & G. Iatrou 2001: Endemic plants of Greece. The Peloponnese. — København. Google Scholar

99.

K. Tesfaye , T. Borsch , K. Govers & E. Bekele 2007: Characterization of Coffea chloroplast microstellites and evidence for the recent divergence of C. arabica and C. eugenioides chloroplast genomes. — Genome 50: 1112–1129. [  CrossRefGoogle Scholar

100.

M. Thulin 1976: Campanula keniensis Thulin sp. nov., and notes on allied species. — Bot. Not. 128: 350– 356. Google Scholar

101.

T. E. Timme , J. V. Kuehl , J. L. Boore & R. K. Jansen 2007: A comparative analysis of the Lactuca and Helianthus (Asteraceae) plastid genomes: identification of divergent regions and categorization of shared repeats. — Amer. J. Bot. 94: 301–312. Google Scholar

102.

N. Toor , G. Hausner & S. Zimmerly 2001 : Coevolution of group II intron RNA structures with their intronencoded reverse transcriptases. — RNA 7: 1142– 1152. [  CrossRefGoogle Scholar

103.

T. G. Tutin 1976: Trachelium. — Pp. 94–95 in: T. G. Tutin , V. H. Heywood , N. A. Burges , D. M. Moore , D. H. Valentine , S. M. Walters & D. A. Webb (ed.), Flora europaea 4. — Cambridge, etc. Google Scholar

104.

S. Wanke , M. A. Jaramillo , T. Borsch , M. S. Samain , D. Quandt & C. Neinhuis 2007: Evolution of the Piperales: matK and trnK intron sequence data reveals a lineage specific resolution contrast. — Molec. Phylogenet. Evol. 42: 477–497. [  CrossRefGoogle Scholar

105.

C. D. Watts , A. E. Fisher , C. D. Shrum , W. L. Newbold , S. Hansen , C. Liu & S. Kelchner 2008: The D4 set: primers that target highly variably intron loops in plant chloroplast geomes. — Molec. Ecol. Notes 8: 1344–1347. Google Scholar

106.

P. Westhoff & R. G. Herrmann 1988: Complex RNA maturation in the chloroplast: the psbB operon from spinach. — Eur. J. Biochem. 171: 551–564. [  CrossRefGoogle Scholar

107.

R. C. Winkworth , J. Lundberg & M. J. Donoghue 2008: Toward a resolution of Campanulid phylogeny, with special reference to the placement of Dipsacales. — Taxon 57: 53–65 Google Scholar

108.

A. Worberg , D. Quandt , A.-M. Barniske , C. Löhne , K. W. Hilu & T. Borsch 2007: Phylogeny of basal eudicots: insights from non-coding and rapidly evolving DNA. — Organisms Diversity Evol. 7: 55–77. [  CrossRefGoogle Scholar

109.

A. Worberg , M. H. Alford , D. Quandt & T. Borsch 2009: Huerteales sister to Brassicales plus Malvales, and newly circumscribed to include Dipentodon, Gerrardina, Huertea, Perrottetia and Tapiscia. — Taxon 58: 468–478. Google Scholar
© 2009 BGBM Berlin-Dahlem.
Thomas Borsch, Nadja Korotkova, Thomas Raus, Wolfram Lobin, and Cornelia Löhne "The petD group II intron as a species level marker: utility for tree inference and species identification in the diverse genus Campanula (Campanulaceae)," Willdenowia 39(1), 7-33, (1 July 2009). https://doi.org/10.3372/wi.39.39101
Published: 1 July 2009
KEYWORDS
chloroplast genome
DNA barcoding
Endemics
Eurasia
molecular evolution
phylogenetic structure
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