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Untangling the hybrid origin of the Chinese tea roses: evidence from DNA sequences of single-copy nuclear and chloroplast genes

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Abstract

The tea-scented China roses largely correspond to the three recognized double-petaled Rosa odorata (Andrews) Sweet (Rosoideae, Rosaceae) varieties, which are the ancestors of modern hybrid tea roses and had a definite and permanent influence on the evolution of modern garden roses. Here the hypothesis of a hybrid origin of the tea-scented China roses between R. odorata var. gigantea and R. chinensis was tested. Two single-copy nuclear genes of the cytosolic glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and the chloroplast-expressed glutamine synthetase (ncpGS) together with two plastid loci (trnL-F and psbA-trnH) were sequenced for representative accessions of four R. odorata varieties, R. chinensis, and 28 other Rosa species. Phylogenetic relationships were estimated from two nuclear loci using maximum parsimony and Bayesian analyses, and a haplotype network was constructed on the combined plastid data using NETWORK. For GAPDH and ncpGS loci, the clonal sequences of the three double-petaled varieties were clustered into two clades, one clade with R. odorata var. gigantea, and the other with partial sequences of R. chinensis, which suggested that the tea-scented China roses were hybrids between R. odorata var. gigantea and R. chinensis. Two plastid loci suggested that R. odorata var. gigantea could be the maternal parent and R. chinensis the paternal parent.

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References

  • Abbott RJ (1992) Plant invasions, interspecific hybridization and the evolution of new plant taxa. Trends Ecol Evol 7:401–405

    Article  PubMed  CAS  Google Scholar 

  • Andrews HC (1810) Roses: or a monograph of the genus Rosa, containing coloured figures of all the known species and beautiful varieties, vol 2. Richard Taylor, London

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford

    Google Scholar 

  • Atienza SG, Torres AM, Millan T, Cubero JI (2005) Genetic diversity in Rosa as revealed by RAPDs. Agric Conspect Sci 70:75–85

    Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Bruneau A, Starr JR, Joly S (2007) Phylogenetic relationships in the genus Rosa: new evidence from chloroplast DNA sequences and an appraisal of current knowledge. Syst Bot 32:366–378

    Article  Google Scholar 

  • Bruun HH (2005) Biological flora of the British Isles. No. 239. Rosa rugosa Thunb. ex Murray. J Ecol 93:441–470

    Article  Google Scholar 

  • Chen H, Morrell PL, de la Cruz M, Clegg MT (2008) Nucleotide diversity and linkage disequilibrium in wild avocado (Persea americana Mill.). J Hered 99:382–389

    Article  PubMed  CAS  Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperms species. Am J Bot 75:1443–1458

    Article  Google Scholar 

  • Crespel L, Chirollet M, Durel CE, Zhang D, Meynet J, Gudin S (2002) Mapping of qualitative and quantitative phenotypic traits in Rosa using AFLP markers. Theor Appl Genet 105:1207–1214

    Article  PubMed  CAS  Google Scholar 

  • Cronn RC, Wendel JF (2003) Cryptic trysts, genomic mergers, and plant speciation. New Phytol 161:133–142

    Article  Google Scholar 

  • Cronn RC, Small RL, Wendel JF (1999) Duplicated genes evolve independently after polyploid formation in cotton. Proc Natl Acad Sci USA 96:14406–14411

    Article  PubMed  CAS  Google Scholar 

  • Cronn RC, Cedroni M, Haselkorn T, Grover C, Wendel JF (2002) PCR-mediated recombination in amplification products derived from polyploid cotton. Theor Appl Genet 104:482–489

    Article  PubMed  CAS  Google Scholar 

  • Curtis W (1794) The botanical magazine, vol 8. Stephen Couchman, London

  • Debener T, Linde M (2009) Exploring complex ornamental genomes: the rose as a model plant. Crit Rev Plant Sci 28:267–280

    Article  CAS  Google Scholar 

  • Debener T, Mattiesch L (1999) Construction of a genetic linkage map of roses using RAPD and AFLP markers. Theor Appl Genet 99:891–899

    Article  CAS  Google Scholar 

  • Debener T, Dohm A, Mattiesch L (2003) Use of diploid self incompatible rose genotypes as a tool for gene flow analyses in roses. Plant Breed 122:285–287

    Article  CAS  Google Scholar 

  • DeBry RW, Olmstead RG (2000) A simulation study of reduced tree-search effort in bootstrap resampling analysis. Syst Biol 49:171–179

    Article  PubMed  CAS  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 

  • Doyle JJ, Doyle JL, Rauscher JT, Brown AHD (2003) Diploid and polyploidy reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytol 161:121–132

    Article  Google Scholar 

  • Emshwiller E, Doyle JJ (1999) Chloroplast-expressed glutamine synthetase (ncpGS): potential utility for phylogenetic studies with an example from Oxalis (Oxalidaceae). Mol Phylogenet Evol 12:310–319

    Article  PubMed  CAS  Google Scholar 

  • Fagerlind F (1944) Kompatibilität und Inkompatibilität in der Gattung Rosa. Acta Horti Berg 13:274–302

    Google Scholar 

  • Fagerlind F (1951) Influence of the pollen-giver on the production of hips, achenes and seeds in the Canina roses. Acta Horti Berg 16:121–168

    Google Scholar 

  • Fagerlind F (1958) Hip and seed formation in newly formed Rosa polyploids. Acta Horti Berg 17:1–27

    Google Scholar 

  • Fei Y, Liu Q, Liu Q, Ge H (2008) Flowers. In: Dong Y, Liu X (eds) Crops and their wild relatives in China. China Agriculture Press, Beijing, pp 184–214

    Google Scholar 

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

    Article  Google Scholar 

  • Ferguson D, Sang T (2001) Speciation through homoploid hybridization between allotetraploids in peonies (Paeonia). Proc Natl Acad Sci USA 98:3915–3919

    Article  PubMed  CAS  Google Scholar 

  • Frajman B, Eggens F, Oxelman B (2009) Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae)—a multigene phylogenetic approach with relative dating. Syst Biol 58:328–345

    Article  PubMed  CAS  Google Scholar 

  • Grant V (1981) Plant speciation. Columbia University Press, New York

    Google Scholar 

  • Grustafsson A (1944) The constitution of the Rosa canina complex. Hereditas 30:405–428

    Article  Google Scholar 

  • Grusz AL, Windham MD, Pryer KM (2009) Deciphering the origins of apomictic polyploids in the Cheilanthes yavapensis Complex (Pteridaceae). Am J Bot 96:1636–1645

    Article  PubMed  CAS  Google Scholar 

  • Gudin S (2000) Rose: genetics and breeding. In: Janick J (ed) Plant breed reviews, vol 17. Wiley, New York, pp 159–189

    Google Scholar 

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

    CAS  Google Scholar 

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–522

    PubMed  CAS  Google Scholar 

  • Hegarty MJ, Hiscock SJ (2005) Hybrid speciation in plants: new insights from molecular studies. New Phytol 165:411–423

    Article  PubMed  CAS  Google Scholar 

  • Howarth DG, Baum DA (2005) Genealogical evidence of homoploid hybrid speciation in an adaptive radiation of Scaevola (Goodeniaceae) in the Hawaiian Islands. Evolution 59:948–961

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hurst CC (1941) Notes on the origin and evolution of our garden roses. J R Hortic Soc 66:242–250

    Google Scholar 

  • Jian HY, Zhang H, Zhang T, Li SF, Wang QG, Yan HJ, Qiu XQ, Tang KX (2010) Karyotype analysis of different varieties of Rosa odorata Sweet. J Plant Genet Resour 11:457–461

    Google Scholar 

  • Joichi A, Yomogida K, Awano K, Ueda Y (2005) Volatile components of tea-scented modern roses and ancient Chinese roses. Flavour Frag J 20:152–157

    Article  CAS  Google Scholar 

  • Joly S, Bruneau A (2006) Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst Biol 55:623–636

    Article  PubMed  Google Scholar 

  • Joly S, Starr JR, Lewis WH, Bruneau A (2006) Polyploid and hybrid evolution in roses east of the Rocky Mountains. Am J Bot 93:412–425

    Article  PubMed  Google Scholar 

  • Kelly LJ, Leitch AR, Clarkson JJ, Hunter RB, Knapp S, Chase MW (2010) Intragenic recombination events and evidence for hybrid speciation in Nicotiana (Solanaceae). Mol Biol Evol 27:781–799

    Article  PubMed  CAS  Google Scholar 

  • Koehne BAE (1893) Deutsche Dendrologie. Ferdinand Enke, Stuttgart

  • Krüssmann G (1981) The complete book of roses. Timber, Portland

    Google Scholar 

  • Krüssmann G (1982) Roses. BT Batsford, London

    Google Scholar 

  • Ku TC, Robertson KR (2003) Rosa. In: Wu ZY, Raven PH (eds) Flora of China, vol 9. Science Press, Beijing, pp 296–339

    Google Scholar 

  • Lewis WH, Basye E (1961) Analysis of nine crosses between diploid Rosa species. Proc Am Soc Hort Sci 78:572–579

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Lihová J, Shimizu KK, Marhold K (2006) Allopolyploid origin of Cardamine asarifolia (Brassicaceae): incongruence between plastid and nuclear ribosomal DNA sequences solved by a single-copy nuclear gene. Mol Phylogenet Evol 39:759–786

    Article  PubMed  Google Scholar 

  • Mercure M, Bruneau A (2008) Hybridization between the escaped Rosa rugosa (Rosaceae) and native R. blanda in eastern North America. Am J Bot 95:597–607

    Article  PubMed  CAS  Google Scholar 

  • Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24:581–583

    Article  PubMed  CAS  Google Scholar 

  • Poke FS, Martin DP, Steane DA, Vaillancourt RE, Reid JB (2006) The impact of intragenic recombination on phylogenetic reconstruction at the sectional level in Eucalyptus when using a single copy nuclear gene (cinnamoyl CoA reductase). Mol Phylogenet Evol 39:160–170

    Article  PubMed  CAS  Google Scholar 

  • Popp M, Erixon P, Eggens F, Oxelman B (2005) Origin and evolution of a circumpolar polyploid species complex in Silene (Caryophyllaceae) inferred from low copy nuclear RNA polymerase introns, rDNA, and chloroplast DNA. Syst Bot 30:302–313

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. http://beast.bio.de.ac.uk/Tracer

  • Rehder A (1940) Manual of cultivated trees and shrubs hardy in North America. Macmillan, New York

    Google Scholar 

  • Rehder A (1949) Bibliography of cultivated trees and shrubs hardy in the cooler temperate regions of the northern hemisphere. Arnold Arboretum of Harvard University, Jamaica Plain

    Google Scholar 

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389

    Article  Google Scholar 

  • Rieseberg LH, Carney SE (1998) Plant hybridisation. New Phytol 140:599–624

    Article  Google Scholar 

  • Rieseberg LH, Wendel JF (1993) Introgression and its consequences in plants. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 70–109

    Google Scholar 

  • Ritz CM, Wissemann V (2011) Microsatellite analyses of artificial and spontaneous dogrose hybrids reveal the hybridogenic origin of Rosa micrantha by the contribution of unreduced gametes. J Hered 102:217–227

    Article  PubMed  CAS  Google Scholar 

  • Roberts AV (1977) Relationship between species in the genus Rosa, section Pimpinellifoliae. Bot J Linn Soc 74:309–328

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Russell A, Samuel R, Klejna V, Barfuss MH, Rupp B, Chase MW (2010) Reticulate evolution in diploid and tetraploid species of Polystachya (Orchidaceae) as shown by plastid DNA sequences and low-copy nuclear genes. Ann Bot 106:37–56

    Article  PubMed  CAS  Google Scholar 

  • Scalliet G, Piola F, Douady CJ, Rety S, Raymond O, Baudino S, Bordji K, Bendahmane M, Dumas C, Cock JM, Hugueney P (2008) Scent evolution in Chinese roses. Proc Natl Acad Sci USA 105:5927–5932

    Article  PubMed  CAS  Google Scholar 

  • Schanzer IA, Kutlunina NA (2010) Interspecific hybridization in wild roses (Rosa L. sect. Caninae DC.). Biol Bull 37:480–488

    Article  Google Scholar 

  • Schanzer IA, Vagina AV (2007) ISSR (Inter Simple Sequence Repeat) markers reveal natural intersectional hybridization in wild roses [Rosa (L.), Sect. Caninae (DC.) Ser. and Sect. Cinnamomeae (DC.) Ser.]. Wulfenia 14:1–14

    Google Scholar 

  • Sweet R (1818) Hortus suburbanus Londinensis: or a catalogue of plants cultivated in the neighbourhood of London. James Ridgway, London

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods), version 4.0b10. Sinauer, Sunderland

    Google Scholar 

  • 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 

  • 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 

  • Wilgenbusch JC, Warren DL, Swofford DL (2004) AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference. http://ceb.csit.fsu.edu/awty

  • Wissemann V (1999) Genetic constitution of Rosa sect. Caninae (R. canina, R. jundzillii) and sect. Gallicanae (R. gallica). Angew Bot 73:191–196

    CAS  Google Scholar 

  • Wissemann V (2003) Conventional taxonomy of wild roses. In: Roberts A, Debener T, Gudin S (eds) Encyclopedia of rose science. Academic, London, pp 111–117

    Chapter  Google Scholar 

  • Wissemann J, Ritz CM (2005) The genus Rosa (Rosoideae, Rosaceae) revisited: molecular analysis of nrITS-1 and atpB-rbcL intergenic spacer (IGS) versus conventional taxonomy. Bot J Linn Soc 147:275–290

    Article  Google Scholar 

  • Wylie AP (1954) The history of garden roses. J R Hortic Soc 79:555–571

    Google Scholar 

  • Yi T, Wen J, Golan-Goldhirsh A, Parfitt DE (2008) Phylogenetics and reticulate evolution in Pistacia (Anacardiaceae). Am J Bot 95:241–251

    Article  PubMed  CAS  Google Scholar 

  • Zielinsky J (1985) Studia nad rodzajem Rosa L. Sistemática sekeji Caninae DC. em. Christ. Arboretum Kornickie 30:3–109

    Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant no. 40830209) and the Knowledge Innovation Program of the Chinese Academy of Sciences (grant no. KSCX2-YW-R-136). We thank Kunming Yang Chinese Rose Gardening Co., Ltd., for supplying the materials of ancient rose cultivars. We thank Prof. Tod Stuessy from the University of Vienna and Prof. Andrew L. Hipps from the Morton Arboretum for revising the manuscript. This work was conducted in the Southwest China Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences.

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Correspondence to De-Zhu Li or Ting-Shuang Yi.

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Meng, J., Fougère-Danezan, M., Zhang, LB. et al. Untangling the hybrid origin of the Chinese tea roses: evidence from DNA sequences of single-copy nuclear and chloroplast genes. Plant Syst Evol 297, 157–170 (2011). https://doi.org/10.1007/s00606-011-0504-5

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