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Natural History, Taxonomy, Biogeography, and Genome Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie der Ludwig-Maximilians-Universität München NATURAL HISTORY, TAXONOMY, BIOGEOGRAPHY AND GENOME EVOLUTION OF THE WORLDWIDE ENDOPARASITE FAMILY APODANTHACEAE (CUCURBITALES) Sidonie Bellot München, 25 Nov. 2014 ii PREFACE Statutory declaration Erklärung Diese Dissertation wurde im Sinne von §12 der Promotionsordnung von Prof. Dr. Susanne S. Renner betreut. Ich erkläre hiermit, dass die Dissertation nicht einer anderen Prüfungskommission vorgelegt worden ist und dass ich mich nicht anderweitig einer Doktorprüfung ohne Erfolg unterzogen habe. Eidesstattliche Erklärung Ich versichere hiermit an Eides statt, dass die vorgelegte Dissertation von mir selbstständig und ohne unerlaubte Hilfe angefertigt wurde. Sidonie Bellot, 25 November 2014 (Unterschrift) 1. Gutachter: Prof. Dr. Susanne S. Renner 2. Gutachter: Prof. Dr. Jochen Heinrichs iii iv Note In this thesis, I present the results from my doctoral research, carried out in Munich from November 2010 to November 2014 under the guidance of Prof. Dr. Susanne S. Renner. My thesis resulted in five manuscripts, presented in Chapters 2 to 6, of which four have been published (Chapters 2, 3, 4 and 6), and one is in review (Chapter 5). I also gave the conference talks listed below. I generated all data and conducted all analyses myself. Writing and discussion involved collaboration with Prof. Dr. Susanne S. Renner. Sidonie Bellot Prof. Susanne S. Renner (Signature) (Signature) List of publications Peer-reviewed journal articles BELLOT, S., AND S. S. RENNER. In review. Intracellular and horizontal transfer of plastid genes to the chondriome – endoparasitism as the precondition for plastome loss. Molecular Biology and Evolution. BELLOT, S., AND S. S. RENNER. 2014. Exploring new dating approaches for parasites: the worldwide Apodanthaceae (Cucurbitales) as an example. Molecular Phylogenetics and Evolution 80: 1–10. BELLOT, S., AND S. S. RENNER. 2014. The systematics of the worldwide endoparasite family Apodanthaceae (Cucurbitales), with a key, a map, and color photos of most species. Phytokeys 30: 41–57. BELLOT, S., AND S. S. RENNER. 2013. Pollination and mating systems of Apodanthaceae and the distribution of reproductive traits in parasitic angiosperms. American Journal of Botany 100: 1083–1094. Book chapter RENNER, S. S., AND S. BELLOT. 2012. Horizontal gene transfer in eukaryotes, focusing on fungi-to-plant and plant-to-plant transfers. Pp. 223-235 in R. Bock & V. Knoop, eds., Genomics of Chloroplasts and Mitochondria. Springer, Heidelberg. v vi Oral presentations BELLOT, S. The evolutionary retention of plastid genomes in non-photosynthetic plants: A comparative approach centred on the endoparasitic Apodanthaceae. Third symposium on the biology of non-weedy parasitic plants. Namur, Belgium, September 12–15, 2013. BELLOT, S. Reconstruction of the chloroplast genome of Spartina maritima, and molecular dating of the divergence between the two genomes reunited in the recent allopolyploid S. anglica. XVIII International Botanical congress IBC 2011. Melbourne, Australia, July 23–30, 2011. BELLOT, S. The complete chloroplast genome of Spartina maritima (Pocaeae, Chloridoideae) using 454 sequencing. BioSystematics Berlin 2011. Berlin, Germany, February 21–27, 2011. Poster RENNER, S. S., AND S. BELLOT. Evolution of the widely distributed endoparasites Apodanthaceae. Radiations 2014. Zürich, Switzerland, June 12 – 15, 2014. Field work Australia, near Perth, August 2011 Zimbabwe, near Harare and Mutare, February 2012 Iran, near Teheran and Isfahan, June 2012 Funding • My research was supported by the Deutsche Forschungs Gemeinschaft (DFG RE 603/16-1). • Travel to attend the 2011 BioSystematics conference in Berlin was funded by an EESLMU Travel Grant. vii viii CONTENTS Preface...............................................................................................................................iii Statutory Declaration..............................................................................................iii Erklärung................................................................................................................iii Eidesstattliche Erklärung........................................................................................iii Note..........................................................................................................................v List of publications..................................................................................................v Oral presentations..................................................................................................vii Fieldwork...............................................................................................................vii Funding..................................................................................................................vii Contents.............................................................................................................................ix Summary............................................................................................................................1 Chapter 1: General Introduction........................................................................................3 Type and phylogenetic occurrence of parasitism in the angiosperms.....................5 Biological traits of parasitic angiosperms……………………………………........6 Substitution rates in the genomes of parasitic angiosperms, and their handling in molecular clock models.......................................................7 The plastid genome of parasitic angiosperms........................................................10 Internal and horizontal gene transfer in parasitic angiosperms..............................12 Background on Apodanthaceae and main research questions................................13 Chapter 2: The systematics of the worldwide endoparasite family Apodanthaceae (Cucurbitales), with a key, a map, and color photos of most species.................................15 Chapter 3: Pollination and mating systems of Apodanthaceae, and the distribution of reproductive traits in parasitic angiosperms..................................41 Chapter 4: Exploring new dating approaches for parasites: the worldwide Apodanthaceae (Cucurbitales) as an example.............................................65 Chapter 5: Intracellular and horizontal transfer of plastid genes to the chondriome – endoparasitism as the precondition for plastome loss.........................................................85 Chapter 6: Horizontal gene transfer in eukaryotes, focusing on fungi-to-plant and plant-to-plant transfers..............................................................................................127 Chapter 7: General Discussion........................................................................................143 Taxonomy of Apodanthaceae...............................................................................145 Biogeography of Apodanthaceae..........................................................................146 Reproductive system of Apodanthaceae...............................................................147 ix x Biological traits of parasitic angiosperms............................................................148 Substitution rates in the genomes of parasitic angiosperms, and their handling in molecular clock models.....................................................150 C-values, chromosome numbers, and plastid genomes of Apodanthaceae.........151 Internal and horizontal transfers in parasitic angiosperms..................................153 General Conclusions......................................................................................................156 References.......................................................................................................................158 Appendix.........................................................................................................................169 Acknowledgements........................................................................................................171 Curriculum Vitae...........................................................................................................173 xi xii SUMMARY This dissertation deals with three key issues in plant evolutionary biology, namely the co-evolution of biological traits, genome evolution, and molecular dating methods. These topics are of particular interest in parasites, which coevolve with their hosts, have highly modified or reduced genomes, often high rates of nucleotide substitutions, and usually no fossil record. To study these topics, I selected the flowering plant family Apodanthaceae (Cucurbitales). Apodanthaceae are endoparasites that live embedded in the stems of their host (Fabaceae or Salicaceae), emerging only in the form of 3-12 mm-long flowers. I revised the taxonomy of the two genera and ten species (Chapter 2) and studied the sexual systems and pollination biology of two species during fieldwork in East Africa and Iran. I also placed key ecological traits of Apodanthaceae in the context of all parasitic angiosperms (focusing on growth form, longevity, pollination, dispersal, and sexual systems) to detect correlations between reproductive traits and parasitism (Chapter 3). I used mitochondrial and nuclear DNA sequences, and molecular clocks, to infer since when Apodanthaceae
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