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Molecular Cytogenetics and Phylogenetic Modeling to Study Chromosome Evolution in the Araceae and Sex Chromosomes in the Cucurbitaceae

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Molecular Cytogenetics and Phylogenetic Modeling to Study Chromosome Evolution in the Araceae and Sex Chromosomes in the Cucurbitaceae Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie der Ludwig-Maximilians-Universität München Molecular Cytogenetics and Phylogenetic Modeling to Study Chromosome Evolution in the Araceae and Sex Chromosomes in the Cucurbitaceae ARETUZA SOUSA DOS SANTOS München, March 2014 1 ii Erstgutachter: Prof. Dr. Susanne Renner Zweitgutachter: Prof. Dr. Günther Heubl Tag der mündlichen Prüfung: 04.06.2014 As minhas famílias, a brasileira e a alemã, e aos meus amigos To my Brazilian and German families and to my friends iii iv 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. Aretuza Sousa dos Santos (Unterschrift) 1. Gutachter: Prof. Dr. Susanne S. Renner 2. Gutachter: Prof. Dr. Günther Heubl v Note In this thesis, I present the results from my doctoral research, carried out in Munich between September 2010 and February 2014 under the guidance of Professor Susanne Renner. The results from my thesis have contributed to four manuscripts presented in Chapters 2 to 5 of which three are published (Chapter 2 to 4) and one is in review (Chapter 5). For the paper presented in Chapter 2, I reviewed all chromosome numbers published for species of Araceae (Appendix and supplementary data Table S1) and contributed to the writing of the discussion, while for the other three papers (Chapters 3 to 5), I generated all data and conducted all analyses myself. Writing and discussion involved collaboration with Susanne Renner. I also presented the seminars and posters listed below. Aretuza Sousa Prof. Susanne S. Renner (Unterschrift) (Unterschrift) Seminars SOUSA, A. February 2012. Using fluorescence in situ hybridization (FISH) to infer the mechanisms responsible for chromosome number changes in the Araceae. Systematic Botany and Mycology Seminar Series – LMU, Munich, Germany. SOUSA, A. October 4-6 2013. From “x” to phylogenetics: Inference of chromosome number evolution in 2013. Summer School in Plant Evolution and Systematics, Bad Feilnbach, Germany. Posters SOUSA, A., CUSIMANO, N. and S.S. RENNER. April 2012. Testing strong predictions about the direction of chromosome evolution in Typhonium. 11th Gatersleben Research Conference on Chromosome Biology, Genome Evolution and Speciation. 23-24 April 2012, Gatersleben, Germany. SOUSA, A., HOLSTEIN, N. and S.S. RENNER. April 2012. Coccinia grandis, the plant with the largest known Y chromosome: Characterizing its male and female karyotypes by FISH. 23-24 April 2012, Gatersleben, Germany. vi List of publications CUSIMANO, N., SOUSA, A. and S.S. RENNER. 2012. Maximum likelihood inference implies a high, not a low, ancestral haploid chromosome number in the Araceae, with a critique of the bias introduced by “x”. Annals of Botany 109: 681 – 692. SOUSA, A., CUSIMANO, N. and S.S. RENNER. 2014. Combining FISH and model-based predictions to understand chromosome evolution in Typhonium (Araceae). Annals of Botany 113: 669 – 680. SOUSA, A. and S.S. RENNER. Descending dysploidy, unusually large interstitial telomere bands, and chromosome evolution in the monocot family Araceae (in review) SOUSA, A., FUCHS, J. and S.S. RENNER. 2013. Molecular Cytogenetics (FISH, GISH) of Coccinia grandis: A ca. 3 myr-old species of Cucurbitaceae with the largest Y/autosome divergence in flowering plants. Cytogenetic and Genome Research 139: 107 – 118. My research was partly funded by: Research Assistant Scholarship, University of Munich (LMU), November 1 to December 31, 2010. Under the auspices of the STIBET scholarship and supported by the DAAD. Deutsche Forschungsgemeinschaft (DFG RE 603/7-1) "Karyotype evolution leading to both extremely high and low chromosome numbers in closely related taxa”. Deutsche Forschungsgemeinschaft (DFG RE 603/6-1 and 6-2) "The evolution of dimorphic sex chromosomes in the genus Coccinia (Cucurbitaceae)”. vii CONTENTS Preface........................................................................................................................................v Statutory Declaration......................................................................................................v Erklärung.........................................................................................................................v Eidesstattliche Erklärung................................................................................................v Note................................................................................................................................vi Seminars…….................................................................................................................vi Posters............................................................................................................................vi List of publications.......................................................................................................vii Funding.........................................................................................................................vii Contents..................................................................................................................................viii Summary................................................................................................................................... 1 Chapter 1: General Introduction............................................................................................... 3 Progress in tree inference, trait reconstruction, and cytogenetics from 1966 to 2014……………………………………………………………..………………..….8 Model-based inference of chromosome evolution, and fluorescence in situ hybridization..………………………………………………………………………...10 Testing model-basal inferences about chromosome evolution with cytogenetic data……………………………………………………………………………….…...14 My study systems and research questions: Araceae and Coccinia...………………....17 References..………………………………………………………………………..…22 Chapter 2: Maximum likelihood inference implies a high, not a low, ancestral haploid chromosome number in the Araceae, with a critique of the bias introduced by “x”.................33 Chapter 3: Combining FISH and model-based predictions to understand chromosome evolution in Typhonium (Araceae)………………………………………………..………..…79 Chapter 4: Descending dysploidy, unusually large interstitial telomere bands, and chromosome evolution in the monocot family Araceae……………………...………….….103 Chapter 5: Molecular Cytogenetics (FISH, GISH) of Coccinia grandis: A ca. 3 myr-old species of Cucurbitaceae with the largest Y/autosome divergence in flowering plants………………………………………………………………………………………...139 viii Chapter 6: General Discussion………..…………………………………………………....153 Chromosome number and phylogenetics: How good is this combination?................154 Molecular cytogenetic data support certain ancestral state reconstructions………...157 Interstitial telomere repeats are not always related to chromosome fusions……...…161 Insights into the sex chromosomes of Coccinia grandis (Curcubitaceae)…………..163 General Conclusions….……………………………………….……….……………….….165 References…..……………………………………………………………….………….…..165 Acknowledgements ...............................................................................................................171 Curriculum Vitae .................................................................................................................172 ix x SUMMARY This study involved the combination of molecular-cytogenetic data and phylogenetic approaches to infer pathways by which chromosome numbers and sizes may have changed during the course of evolution. The two systems for which I generated new data are the monocot plant family Araceae and Coccinia, a genus of Cucurbitaceae. Araceae have about 3800 species in 118 genera, and chromosome numbers range from 2n = 168 to 2n = 8, the latter the lowest number so far and newly reported in my study. The small genus Coccinia includes C. grandis, with the largest known Y chromosome in plants, as documented in my work. The thesis comprises four published or submitted papers. The first paper reports the result of phylogenetic modeling of chromosome number change along a phylogeny for the Araceae with 113 genera represented. I used a maximum likelihood approach to find the most likely combination of events explaining today’s chromosome numbers in the 113 genera. The permitted events were chromosome gains (i.e. breaks), losses (i.e. fusions), doubling (polyploidization), or fusion of gametes with different ploidy. The best-fitting model inferred an ancestral haploid number of 16 or 18, higher than previously suggested numbers, a large role for chromosome fusion, and a limited role of polyploidization. The sparse taxon sampling and deep age (at least 120 Ma) of the events near the root of Araceae caution against placing too much weight on “ancestral” numbers, but inferred events in more closely related species can be tested with cytogenetic methods, which I did in two further studies (papers 2 and 3). I selected Typhonium, with 50-60 species, a range of 2n = 8 to 2n = 65 chromosomes. The family-wide study had suggested a reduction
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