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A molecular phylogenetic study of Hemsleya (Cucurbitaceae) based on ITS, rpl16, trnH-psbA, and trnL DNA sequences

Abstract

This paper presents the first molecular phylogeny of the genus Hemsleya using nuclear ITS and plastid trnH-psbA, rpl16, and trnL DNA sequences to examine the relationships among Hemsleya species. Phylogenetic relationships were elucidated using a combined analysis of all four datasets, however, the number of parsimony-informative characters was still insufficient to resolve all relationships. Parsimony and Bayesian trees were highly congruent. Twenty-three species of Hemsleya split into two major clades corresponding to two subgenera, i.e., subg. Graciliflorae and subg. Hemsleya. These results are partly in agreement with Li’s sectional classification. However, the molecular data are inconsistent with Li’s classification at the subsectional level. The molecular phylogeny revealed a striking overall correlation between the phylogenetic relationships of the species and their geographical distribution. The Kangdian ancient landmass could be the center of origin of the genus.

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References

  • Bremer B, Jansen RK, Oxelman B, Backlund M, Lantz H, Kim KJ (1999) More characters or more taxa for a robust phylogeny: case study from the coffee family (Rubiaceae). Syst Biol 48:413–435

    Article  CAS  PubMed  Google Scholar 

  • Burland TG (2000) DNASTAR’s Lasergene sequence analysis software. Methods Mol Biol 132:71–91

    CAS  PubMed  Google Scholar 

  • Chen S-K (1995) A classificatory system and geographical distribution of the genus Gynostemma Bl (Cucurbitaceae). Acta Phytotax Sin 33:403–410

    Google Scholar 

  • Chen Y, Chiu M-H, Gu K, Li Z-R (2003) Cucurbitacin and triterpenoid glycosides from Hemsleya gigantha. Chin Chem Lett 14:475–478

    CAS  Google Scholar 

  • Chiu M-H, Gao J (2003) Three new cucurbitacins from Hemsleya lijiangensis. Chin Chem Lett 14:389–392

    CAS  Google Scholar 

  • Chung SM, Decker-Walters DS, Staub JE (2003) Genetic relationships within the Cucurbitaceae as assessed by ccSSR marker and sequence analyses. Can J Bot 81:814–832

    Article  CAS  Google Scholar 

  • Chung SM, Staub JE, Chen JF (2006) Molecular phylogeny of Cucumis species as revealed by consensus chloroplast SSR marker length and sequence variation. Genome 49:219–229

    Article  CAS  PubMed  Google Scholar 

  • Clarke AC, Burtenshaw MK, McLenachan PA, Erickson DL, Penny D (2006) Reconstructing the origins and dispersal of the polynesian bottle gourd (Lagenaria siceraria). Mol Biol Evol 23:893–900

    Article  CAS  PubMed  Google Scholar 

  • Decker-Walters DS, Walters TW, Posluszny U, Kevan PG (1990) Genealogy and gene flow among annual domesticated species of Cucurbita. Can J Bot 68:782–789

    Article  Google Scholar 

  • Dinan L, Whiting P, Sarker SD, Kasai R, Yamasaki K (1997) Cucurbitane-type compounds from Hemsleya carnosiflora antagonize ecdysteroid action in the Drosophila melanogaster BII cell line. Cell Mol Life Sci 53:271–274

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1994) Testing significance of incongruence. Cladistics 10:315–319

    Article  Google Scholar 

  • Farris JS, Källersjö M, Kluge AG, Bult C (1995) Constructing a significance test for incongruence. Syst Biol 44:570–572

    Google Scholar 

  • Forbes FB, Hemsley WB (1888) Index florae sinensis. J Linn Soc Lond Bot 23:490

    Google Scholar 

  • Ganal M, Hemleben V (1986) Comparison of the ribosomal RNA genes in four closely related Cucurbitaceae. Pl Syst Evol 154:63–77

    Article  CAS  Google Scholar 

  • Garcia-Mas J, Monforte AJ, Arús P (2004) Phylogenetic relationships among Cucumis species based on the ribosomal internal transcribed spacer sequence and microsatellite markers. Pl Syst Evol 248:191–203

    Article  CAS  Google Scholar 

  • Graybeal A (1998) Is it better to add taxa or characters to a difficult phylogenetic problem? Syst Biol 47:9–17

    Article  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Hano Y, Shi Y-Q, Taro Nomura, Yang P-Q, Chang W-J (1997) Two acetogenins from Hemsleya ellipsoidea. Phytochemistry 46:1447–1449

    Article  CAS  Google Scholar 

  • Hillis DM (1998) Taxonomic sampling, phylogenetic accuracy, and investigator bias. Syst Biol 47:3–8

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Jarret RL, Newman M (2000) Phylogenetic relationships among species of Citrullus and the placement of C. rehmii De Winter as determined by internal transcribed spacer (ITS) sequence heterogeneity. Genet Resour Crop Evol 47:215–222

    Article  Google Scholar 

  • Jeffrey C (1980a) A review of the Cucurbitaceae. Bot J Linn Soc 81:233–247

    Article  Google Scholar 

  • Jeffrey C (1980b) The Cucurbitaceae of Eastern Asia. Royal Botanic Gardens, Kew

  • Jeffrey C (1990) Systematics of the Cucurbitaceae: an overview. In: Bates DM, Robinson RW, Jeffrey C (eds) Biology and utilization of the Cucurbitaceae. Cornell University Press, Ithaca, p 3–28

  • Jeffrey C (2005) A new system of Cucurbitaceae. Bot Zhurn 90:332–335

    Google Scholar 

  • Jobst J, King K, Hemleben V (1998) Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of the family Cucurbitaceae. Mol Phylogenet Evol 9:204–219

    Article  CAS  PubMed  Google Scholar 

  • Jordan WC, Courtney MW, Neigel JE (1996) Low levels of intraspecific genetic variation at a rapidly evolving chloroplast DNA locus in North American duckweeds (Lemnaceae). Am J Bot 83:430–439

    Article  CAS  Google Scholar 

  • King K, Torres RA, Zentgraf U, Hemleben V (1993) Molecular evolution of the intergenic spacer in the nuclear ribosomal RNA genes of Cucurbitaceae. J Mol Evol 36:144–152

    Article  CAS  PubMed  Google Scholar 

  • Kocyan A, Zhang L-B, Schaefer H, Renner SS (2007) A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Mol Phylogenet Evol 44:553–577

    Article  CAS  PubMed  Google Scholar 

  • Kress WJ, Erickson DL (2007) A two-locus global DNA barcode for land plants: the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS ONE 2(6): e508. doi:10.1371/journal.pone.0000508

  • Kress JW, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH (2005) Use of DNA barcodes to identify flowering plants. Proc Natl Acad Sci USA 102:8369–8374

    Article  CAS  PubMed  Google Scholar 

  • Li D-Z (1993) Systematics and evolution of Hemsleya (Cucurbitaceae). Yunnan Science and Technology Press, Kunming

  • Lin Y-P, Chiu M-H, Li Z-R (2003) Two new compounds from Hemsleya penxianensis var. gulinensis. Chin Chem Lett 14:169–172

    CAS  Google Scholar 

  • Lu A-M (1982) Material for the genus Hemsleya Cogn. Acta Phytotax Sin 20:87–90

    Google Scholar 

  • Montes-Hernández S, Eguiarte LE (2002) Genetic structure and indirect estimates of gene flow in three taxa of Cucurbita (Cucurbitaceae) in western Mexico. Am J Bot 89:1156–1163

    Article  Google Scholar 

  • Ng TJ (1993) New opportunities in the Cucurbitaceae. In: Janick J, Simon JE (eds) New crops. Wiley, New York, pp 538–546

    Google Scholar 

  • Nie R-L, Chen Z-L (1986) The research history and present status on the chemical components of genus Hemsleya (Cucurbitaceae). Acta Bot Yunnan 8:115–124

    CAS  Google Scholar 

  • Nie R-L, Kasai R, Kasai R (1984) Saponins from Chinese medical plants. I. Isolation and structures of hemsloisides. Planta Med 50:322–327

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Qiu M-H, Chen S-K, Chen J-C, Zhou L, Li Z-R, Nie R-L (2005) Chemotaxonomy of Cucurbitaceae. Chin J Appl Environ Biol 11:673–685

    CAS  Google Scholar 

  • Rannala B, Yang ZH (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  CAS  PubMed  Google Scholar 

  • Reeves G, Chase M, Goldblatt P, Rudall P, Fay M, Cox A, Lejeune B, Chies TDE (2001) Molecular systematics of Iridaceae: evidence from four plastid DNA regions. Am J Bot 88:2074–2087

    Article  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA-polymerase. Science 239:487–491

    Article  CAS  PubMed  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  CAS  Google Scholar 

  • Sanjur OJ, Piperno DR, Andres TC, Wessel-Beaver L (2002) Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: implications for crop plant evolution and areas of origin. Proc Natl Acad Sci USA 99:535–540

    Article  CAS  PubMed  Google Scholar 

  • Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166

    Article  CAS  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence based phylogenetic analyses. Syst Biol 49:369–381

    Article  CAS  PubMed  Google Scholar 

  • Soltis DE, Soltis PS, Mort ME, Chase MW, Savolainen V, Hoot SB, Morton M (1998) Inferring complex phylogenies using parsimony: an empirical approach using three large DNA data sets for angiosperms. Syst Biol 47:32–42

    Article  CAS  PubMed  Google Scholar 

  • Suzuki Y, Glazko GV, Nei M (2002) Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc Natl Acad Sci USA 99:16138–16143

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2001) PAUP*. Phylogenetic analysis using parsimony and other methods 4.0b10. Sinauer Associates, Sunderland

    Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Vischi M, Arzenton F, De Paoli E, Paselli S, Tomat E, Olivieri AM (2006) Identification of wild species of sunflower by a specific plastid DNA sequence. Helia 45:11–18

    Article  Google Scholar 

  • White TJ, 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 application. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wiens JJ (1998) Combining data sets with different phylogenetic histories. Syst Biol 47:568–581

    Article  CAS  PubMed  Google Scholar 

  • Wilcox TP, Zwickl DJ, Heath TA, Hillis DM (2002) Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Mol Phylogenet Evol 25:361–371

    Article  CAS  PubMed  Google Scholar 

  • Wilson HD, Doebley J, Duvall M (1992) Chloroplast DNA diversity among wild and cultivated members of Cucurbita (Cucurbitaceae). Theor Appl Genet 84:859–865

    Article  CAS  Google Scholar 

  • Wortley AH, Rudall PJ, Harris DJ, Scotland RW (2005) How much data are needed to resolve a difficult phylogeny? Case study in Lamiales. Syst Biol 54:697–709

    Article  PubMed  Google Scholar 

  • Wu C-Y, Chen Z-L (1985) Materia and floram Cucurbitacearum Sinensium–Hemsleya Cogn. Acta Phytotax Sin 23:121–143

    Google Scholar 

  • Wu C-Y, Chen Z-L (1986) Flora reipublicae popularis sinicae, vol 73. Science Press, Beijing, pp 102–129

  • Wu C-Y, Wu S-G (1998) A proposal for a new floristic kingdom (realm): the E. Asiatic kingdom, its delimitation and characteristics. In: Zhang AL, Wu SG (eds) Proceedings of the first international symposium on floristic characteristics and diversity of East Asian plants. China Higher Education Press/Springer, Beijing/Berlin, pp 3–42

    Google Scholar 

  • Wu J, Wu Y, Yang B-B (2002) Anticancer activity of Hemsleya amabilis extract. Life Sci 71:2161–2170

    Article  CAS  PubMed  Google Scholar 

  • Yang Y-K, Chiu M-H, Gao C-W, Nie R-L, Lu Y, Zheng Q-T (2000) The novel structure of a disaccharide derivative from Hemsleya amabilis. Tetrahedron 56:7433–7435

    Article  CAS  Google Scholar 

  • Yoder AD, Irwi JA, Payseur BA (2001) Failure of the ILD to determine data combinability for slow loris phylogeny. Syst Biol 50:408–424

    Article  CAS  PubMed  Google Scholar 

  • Zhang L-B, Simmons MP, Kocyan A, Renner SS (2006) Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Mol Phylogenet Evol 39:305–322

    Article  CAS  PubMed  Google Scholar 

  • Zhou T-R (1984) Physico-geography of China: palaeogeography, vol 1. Science Press, Beijing

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Acknowledgments

The research was supported by the National Basic Research Program of China (973 program, grant no. 2007CB411601) and the National Natural Science Foundation of China (grant 40830209). The authors are extremely grateful to J.K. Triplett (Iowa State University), Dr. Lian-Ming Gao, Dr. Ting-Shuang Yi, and Dr. Jin-Mei Lu (KIB) for their valuable comments to help improve the manuscript.

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Correspondence to De-Zhu Li.

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Li, HT., Yang, JB., Li, DZ. et al. A molecular phylogenetic study of Hemsleya (Cucurbitaceae) based on ITS, rpl16, trnH-psbA, and trnL DNA sequences. Plant Syst Evol 285, 23–32 (2010). https://doi.org/10.1007/s00606-009-0252-y

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  • DOI: https://doi.org/10.1007/s00606-009-0252-y

Keywords

  • Hemsleya
  • Molecular phylogeny
  • Biogeography
  • ITS
  • trnH-psbA
  • rpl16
  • trnL