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Subfamilial and tribal relationships of Ranunculaceae: evidence from eight molecular markers

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Abstract

The first molecular phylogenies of the flowering plant family Ranunculaceae were published more than twenty years ago, and have led to major changes in the infrafamilial classification. However, the current phylogeny is not yet well supported, and relationships among subfamilies and tribes of Ranunculaceae remain an open question. Eight molecular markers from the three genomes (nuclear, chloroplast and mitochondrial) were selected to investigate these relationships, including new markers for the family (two homologs of the nuclear CYCLOIDEA gene, the chloroplast gene ndhF, and the mitochondrial intron nad4-I1). The combination of multiple markers led to better resolution and higher support of phylogenetic relationships among subfamilies of Ranunculaceae, and among tribes within subfamily Ranunculoideae. Our results challenge the monophyly of Ranunculoideae as currently circumscribed due to the position of tribe Adonideae (Ranunculoideae), sister to Thalictroideae. We suggest that Thalictroideae could be merged with Ranunculoideae in an enlarged single subfamily.

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Acknowledgments

This work was supported by a grant from Agence Nationale de la Recherche [ANR-07-BLAN-0112-02] and by a grant from Institut Diversité Ecologie Evolution du Vivant (2011–2012). We thank Olivier Chauveau for technical assistance with the sequencing and for helpful discussions, and Bruno Lascaux for helping us to collect plant material in Orsay. We also thank the Royal Botanic Garden Edinburgh for permission to collect material, and Fiona Inches for assistance with the sampling.

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Author notes

  1. Guillaume Cossard

    Present address: Department of Ecology and Evolution, University of Lausanne, Biophore Building, 1015, Lausanne, Switzerland

Authors and Affiliations

  1. Université Paris Sud, Laboratoire Ecologie, Systématique, Evolution, CNRS UMR 8079-AgroParisTech, 91405, Orsay, France

    Guillaume Cossard, Julie Sannier, Hervé Sauquet & Sophie Nadot

  2. CNRS, UMR 0320/UMR 8120 Génétique Quantitative et Evolution-Le Moulon, 91190, Gif-Sur-Yvette, France

    Guillaume Cossard, Julie Sannier & Catherine Damerval

  3. Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh, EH3 5LR, UK

    Louis Ronse de Craene

  4. Institut de Systématique, Evolution, Biodiversité, ISYEB-UMR 7205 CNRS-MNHN-UPMC-EPHE, Muséum national d’histoire naturelle, Sorbonne Universités, 57 rue Cuvier CP39, 75005, Paris, France

    Florian Jabbour

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Handling editor: Alexandra Nora Muellner-Riehl.

Electronic supplementary material

606_2015_1270_MOESM1_ESM.pdf

Online Resource 1. Voucher information and GenBank accession numbers of the sequences used in this study. PBL: Parc Botanique de Launay(F), JBL: Jardin Botanique de Lyon (France), JBVP: Jardin Botanique de la Ville de Paris (F), RBGE: Royal Botanic Garden Edinburgh (UK),BFAG: Betty Ford Alpine Gardens (USA, Colorado), ROST: Botanischer Garten Rostock (D), GEISS: Botanischer Garten Giessen (F), JS:collected by Julie Sannier (wild or commercial origin). Voucher information is given only for the newly generated sequences (PDF 856 kb)

Online Resource 2. List of primers used in this study and PCR conditions followed for mostof the samples (PDF 1696 kb)

606_2015_1270_MOESM3_ESM.pdf

Online Resource 3. Schematic representation of the DNA regions sequenced in this study andof the primers used.A. The matK region divided into three parts, 3’trnK-matK intron, matK gene and matK-5’trnKintron. B. The ndhF region. C. Part of the nad4-I1 intronic region. Coding parts are in gray,non-coding regions are represented by straight lines. Primers are represented by arrows. Theintron 1 of subunit IV of NADH dehydrogenase was only partially amplified. Dashed linessymbolise the rest of the intron. D. The CYCLOIDEA-like region with primers represented byarrows (PDF 3236 kb)

606_2015_1270_MOESM4_ESM.pdf

Online Resource 4. PMaximum likelihood tree obtained from the combined alignment of CYC1 and CYC2 sequences showing the two paralogous lineages (PDF 319 kb)

606_2015_1270_MOESM5_ESM.pdf

Online Resource 5. Bayesian inference cladogram of the Ranunculaceae obtained from the matK dataset.Numbers above branches are Bayesian posterior probabilities (>0.5) and ML bootstrap percentages (>50%). Subfamilies and tribes are according to the classification of Wang et al. (2009) (PDF 432 kb)

606_2015_1270_MOESM6_ESM.pdf

Online Resource 6. Bayesian inference cladogram of the Ranunculaceae obtained from the ndhF dataset.Description: Numbers above branches are Bayesian posterior probabilities (>0.5) and ML bootstrap percentages (>50%). Subfamilial and tribal classification is based on Wang et al. (2009). Stars indicate nodes that are not found in ML tree (PDF 428 kb)

606_2015_1270_MOESM7_ESM.pdf

Online Resource 7. Bayesian inference cladogram of the Ranunculaceae obtained from the rbcL dataset.Description: Numbers above branches are Bayesian posterior probabilities (>0.5) and ML bootstrap percentages (>50%). Subfamilial and tribal classification is based on Wang et al. (2009). Stars indicate nodes that are not found in ML tree (PDF 436 kb)

606_2015_1270_MOESM8_ESM.pdf

Online Resource 8. Bayesian inference cladogram of the Ranunculaceae obtained from the trnL dataset.Description: Numbers above branches are Bayesian posterior probabilities (>0.5) and ML bootstrap percentages (>50%). Subfamilial and tribal classification is based on Wang et al. (2009). Stars indicate nodes that are not found in ML tree (PDF 427 kb)

606_2015_1270_MOESM9_ESM.pdf

Online Resource 9. Bayesian inference tree obtained from the combined analysis of all chloroplast markers (matK, ndhF, rbcL, trnL).Description: Numbers above branches are Bayesian posterior probabilities (>0.5) and bootstrap percentages (>50%). Subfamilies and tribes are according to the classification of Wang et al. (2009). Stars indicate nodes that are not found in the ML tree (PDF 433 kb)

606_2015_1270_MOESM10_ESM.pdf

Online Resource 10. Bayesian inference cladogram of the Ranunculaceae obtained from the nad4-I1 dataset.Description: Numbers above branches are Bayesian posterior probabilities (>0.5) and ML bootstrap percentages (>50%). Subfamilies and tribes are according to the classification of Wang et al. (2009) (PDF 446 kb)

606_2015_1270_MOESM11_ESM.pdf

Online Resource 11. Bayesian inference tree obtained from the ITS dataset.Description: Numbers above branches are Bayesian posterior probabilities (>0.5) andbootstrap percentages (>50%). Subfamilies and tribes are according to the classification ofWang et al. (2009). Stars indicate nodes that are not found in the ML tree (PDF 417 kb)

606_2015_1270_MOESM12_ESM.pdf

Online Resource 12. Bayesian inference tree obtained from the combined analysis of nuclearmarkers (ITS, RanaCYL1, RanaCYL2).Description: Numbers above branches are Bayesian posterior probabilities (>0.5) andbootstrap percentages (>50%). Bootstrap support values lower than 50% are replaced bydashes. Subfamilies and tribes are according to the classification of Wang et al. (2009). Starsindicate nodes that are not found in the ML tree (PDF 493 kb)

606_2015_1270_MOESM13_ESM.pdf

Online Resource 13. Bayesian inference phylogram obtained from the total evidence datasetincluding all markers.Description: Numbers above the branches are Bayesian posterior probabilities and bootstrappercentages (>50%). Subfamilies and tribes are according to the classification of Wang et al.(2009). Stars indicate nodes that are not found in ML tree (PDF 438 kb)

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online Resource 1. Voucher information and GenBank accession numbers of the sequences used in this study.

Online Resource 2. List of primers used in this study and PCR conditions followed for most of the samples.

Online Resource 3. Schematic representation of the DNA regions sequenced in this study and of the primers used.

Online Resource 4. Maximum likelihood tree obtained from the combined alignment of CYC1 and CYC2 sequences showing the two paralogous lineages.

Online Resource 5. Bayesian inference cladogram of the Ranunculaceae obtained from the matK dataset.

Online Resource 6. Bayesian inference cladogram of the Ranunculaceae obtained from the ndhF dataset.

Online Resource 7. Bayesian inference cladogram of the Ranunculaceae obtained from the rbcL dataset.

Online Resource 8. Bayesian inference cladogram of the Ranunculaceae obtained from the trnL dataset.

Online Resource 9. Bayesian inference tree obtained from the combined analysis of all chloroplast markers (matK, ndhF, rbcL, trnL).

Online Resource 10. Bayesian inference cladogram of the Ranunculaceae obtained from the nad4-I1 dataset.

Online Resource 11. Bayesian inference tree obtained from the ITS dataset.

Online Resource 12. Bayesian inference tree obtained from the combined analysis of nuclear markers (ITS, RanaCYL1, RanaCYL2).

Online Resource 13. Bayesian inference phylogram obtained from the total evidence dataset including all markers.

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Cossard, G., Sannier, J., Sauquet, H. et al. Subfamilial and tribal relationships of Ranunculaceae: evidence from eight molecular markers. Plant Syst Evol 302, 419–431 (2016). https://doi.org/10.1007/s00606-015-1270-6

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