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A Bioinformatic Approach to Unravel Highly Complex Cereal Genomes

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Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt Lehrstuhl für Genomorientierte Bioinformatik GenomeZipper - a bioinformatic approach to unravel highly complex cereal genomes Mihaela-Maria Martis VollständigerAbdruck der von der Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt der Technischen Universität München zur Erlangung des akade- mischen Grades eines Doktors der Naturwissenschaften (Dr. rer. nat.) genehmigten Dissertation. Vorsitzender: Univ.-Prof. Dr. Claus Schwechheimer Prüfer der Dissertation: 1. Univ.-Prof. Dr. Hans-Werner Mewes 2. Univ.-Prof. Dr. Chris-Carolin Schön Die Dissertation wurde am 23.03.2015 bei der Technischen Universität München eingereicht und durch die Fakultät Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt am 27.05.2015 angenommen. Abstract Cereals belong to one of the most economically important plant families (Poaceae). They provide half of all the calories consumed by humans, are indispensable for animal feed and the beverage industry, and have a huge potential to be used for biofuel production. Until recently, most whole genome sequencing projects were restricted to small plant genomes. Large and complex grass genomes, including those of barley (Hor- deum vulgare), rye (Secale cereale), and wheat (Triticum aestivum), were limited by computational requirements in sequencing, genome assembly, and identification of protein coding regions. The new next-generation sequencing technologies enabled to tackle these larger genomes. However, the assemblies are still highly fragmented and lack positional ordering. This thesis describes a new tool termed GenomeZipper, which aims to identify, or- der and structure chromosomal survey sequences of large grass genomes that lack physical maps by exploiting the widely conserved synteny among grasses. Addi- tionally, subsequent comparative analyses performed on the GenomeZipper results are described. Applied on barley (Hordeum vulgare) and rye (Secale cereale) the GenomeZipper concept allowed to arrange and orient 68% and 72% of the estimated gene space, respectively. The resulting linear ordered gene maps were used to compare the con- served gene structure and organisation in these grasses. The comparison revealed several major chromosomal rearrangements in the rye genome and molecular cha- racteristics gave evidence for introgressive hybridisation. This indicates that the rye genome evolution and speciation was influenced by reticulate evolution. Another structural characteristic of the rye genome studied in this thesis are su- pernumerary B chromosomes (Bs). Bs are dispensable extra chromosomes to the normal chromosome complement (A chromosomes), which exhibit non-Mendelian inheritance. This work highlights the intraspecific origin of Bs by recombination of two A chromosomes (3R and 7R) and give insights into their evolution and compo- sition. Large amount of organellar DNA, B specific repeats and large numbers of gene fragments appear to be characteristic for the B chromosomes of rye. Zusammenfassung Süßgräser (Poaceae) sind eine weltweit verbreitete und wirtschaftlich bedeutende Pflanzenfamilie, zu denen auch Getreide gehören. Sie liefern über die Hälfte der Kalorien für die Welternährung und sind als Futterpflanze und als Rohstoff für die Brauindustrie unverzichtbar. Dazu gewinnen sie zunehmend an Bedeutung im Be- reich der Biokraftstoffproduktion. Auf Grund von technischen und finanziellen Einschränkungen wurden zunächst nur Pflanzen mit relativ kleinen Genomen zur Sequenzierung ausgewählt. Die Sequen- zierung, Assemblierung und Gendetektion in großen und komplexen Gräsergenomen, wie Gerste (Hordeum vulgare), Roggen (Secale cereale) und Weizen (Triticum aes- tivum), waren bisher durch die großen notwendigen Rechenleistungen eingeschränkt. Durch den Einsatz neuer Next-Generation-Sequencing-Technologien wurde ein Durch- bruch erzielt und die Analyse solch großer Genome möglich. Dennoch sind diese Genome noch unvollständig und die Abfolge ihrer Sequenzen weitgehendst un- bekannt. Im Rahmen dieser Arbeit wird eine neue Methode vorgestellt, die als GenomeZipper bezeichnet wird. Das GenomeZipper-Konzept nutzt die konservierte Syntänie zwi- schen Gräser aus, um Gensequenzen von Grassgenomen, ohne physikalische Karte, entlang von Chromosomen anzuordnen. Zusätzlich werden die Ergebnisse der ver- gleichenden Analysen, welche auf den vom GenomeZipper erstellten virtuellen Genkarten beruhen, beschrieben. Das GenomeZipper-Verfahren wurde auf unter- schiedliche Gräser, wie Gerste und Roggen, angewandt, wobei für respektive 68% und 72% der geschätzten Gene die Reihenfolge entlang der Chromosomen be- stimmt werden konnte. Der Vergleich der daraus entstandenen virtuellen Gerste- und Roggengenkarten enthüllte wesentliche chromosomale Änderungen der Anord- nung im Roggengenom. Diese deuten darauf hin, dass die Roggen-Artbildung und -Evolution durch introgressive Hybridisierung und retikuläre Evolution sowie einer Reihe von Genomduplikationen beeinflusst wurde. Ein weiterer Bestandteil dieser Arbeit ist die Analyse von B Chromosomen (Bs) in Roggen. Bs sind überzählige, entbehrliche Chromosomen, die unabhängig von den Mendelschen Gesetzen vererbt werden. Die Ergebnisse dieser Arbeit zeigen den intraspezifischen Ursprung der Roggen B Chromosomen durch Fusion zweier A Chromosomen (3R und 7R) und geben Einblicke in die Evolution sowie die Zusammensetzung der B Chromosomen. Ansammlungen von Organellen-DNA, B- spezifischen repetitiven Sequenzen und Genfragmenten scheinen charakteristisch für die B Chromosomen in Roggen zu sein. Acknowledgements First of all, I wish to thank my supervisors at the Institute of Bioinformatics and Systems Biolo- gy, Dr. Klaus Mayer and Prof. Dr. Hans-Werner Mewes, for giving me the opportunity to pursue a PhD. I especially appreciate the support and guidance given by Dr. Klaus Mayer concerning my work at the Plant Genome and Systems Biology group as well as the chance to travel and present my research at international conferences. Special thanks go to Dr. Andreas Houben for introducing me to the fascinating research area on B chromosomes. Thank you for your patience, support, and comments regarding the rye B chromosomes and for the opportunity to present my results on the 3rd B-Chromosome Confe- rence. Thanks to everyone at PGSB for the good teamwork and constructive feedback, for lunch breaks, and for supporting my chili and tomato breeding attempt. It has been a great honor and pleasure to collaborate with you on different projects. To Heidrun for her input, feedback, and support over the last years, for Christmas baking, and for skiing and sleigh rides. To all my friends and family, for good times, encouragements, and shoulders to cry on. To Hanna and Anna, for both exhaustive and last-minute proofreading. Without you I would have lost the day against English grammar. My warmest thanks go to Bernhard. Thank you for supporting and encouraging me through a challenging time. I would have never ever finished my thesis without you. It is good to have you by my side. i Abbreviations Ae Aegilops AFLP amplified fragment-length polymorphism BAC bacterial artificial chromosomes BBH bi-directional Blast hit Bd Brachypodium distachyon BLAST basic local alignment search tool bp base pairs BP before present cal calibrated CSS chromosomal survey sequences DNA deoxyribonucleic acid EST expressed sequence tag FHIT fragile histidine triad gene FISH fluorescence in situ hybridisation fl-cDNA full-length complementary DNA Gbp giga base pairs GSS genome survey sequences IRAP inter-retrotransposon amplified polymorphism ITS internal transcribed spacers ISSR inter-simple sequence repeat kbp kilo base pairs LTR long terminal repeat Mbp mega base pairs Mya million years ago NGS next generation sequencing NOR nuclear organising regions Os Oryza sativa (rice) PSR paternal-sex-ratio qPCR quantitative polymerase chain reaction rDNA ribosomal DNA RFLP restriction fragment length polymorphism RNA ribonucleic acid Sb Sorghum bicolor (sorghum) Sc Secale cereale (rye) sSMC small supernumerary marker chromosomes TE transposable elements iii Abbreviations WCS whole chromosome shotgun WGS whole genome shotgun WGD whole genome duplication YAML yet another multicolumn layout (a human-readable data serialization standard) iv List of publications The following peer-reviewed publications are included in this thesis: 1. Mayer KF, Taudien S, Martis M, Šimková H, Suchánková P, Gundlach H, Wicker T, Petzold A, Felder M, Steuernagel B, Scholz U, Graner A, Platzer M, Doležel J and Stein N. Gene content and virtual gene order of barley chromosome 1H. Plant Physiol. 2009 Oct, 151(2):496-505. doi:10.1104/pp.109.142612. 2. Mayer KF, Martis M, Hedley PE, Šimková H, Liu H, Morris JA, Steuernagel B, Taudien S, Roessner S, Gundlach H, Kubaláková M, Suchánková P, Murat F, Felder M, Nuss- baumer T, Graner A, Salse J, Endo T, Sakai H, Tanaka T, Itoh T, Sato K, Platzer M, Matsumoto T, Scholz U, Doležel J, Waugh R and Stein N. Unlocking the barley genome by chromosomal and comparative genomics. Plant Cell. 2011 Apr, 23(4):1249-63. doi: 10.1105/tpc.110.082537. 3. Martis MM, Klemme S, Banaei-Moghaddam AM, Blattner FR, Macas J, Schmutzer T, Scholz U, Gundlach H, Wicker T, Šimková H, Novák P, Neumann P, Kubaláková M, Bauer E, Haseneyer G, Fuchs J, Doležel J, Stein N, Mayer KF and Houben A. Selfish supernumerary chromosome reveals its origin as a mosaic of host genome and organellar sequences. PNAS. 2012 Aug, 14;109(33):13343-6. doi:10.1073/pnas.1204237109.
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  • Complete List of Literature Cited* Compiled by Franz Stadler

    Complete List of Literature Cited* Compiled by Franz Stadler

    AppendixE Complete list of literature cited* Compiled by Franz Stadler Aa, A.J. van der 1859. Francq Van Berkhey (Johanes Le). Pp. Proceedings of the National Academy of Sciences of the United States 194–201 in: Biographisch Woordenboek der Nederlanden, vol. 6. of America 100: 4649–4654. Van Brederode, Haarlem. Adams, K.L. & Wendel, J.F. 2005. Polyploidy and genome Abdel Aal, M., Bohlmann, F., Sarg, T., El-Domiaty, M. & evolution in plants. Current Opinion in Plant Biology 8: 135– Nordenstam, B. 1988. Oplopane derivatives from Acrisione 141. denticulata. Phytochemistry 27: 2599–2602. Adanson, M. 1757. Histoire naturelle du Sénégal. Bauche, Paris. Abegaz, B.M., Keige, A.W., Diaz, J.D. & Herz, W. 1994. Adanson, M. 1763. Familles des Plantes. Vincent, Paris. Sesquiterpene lactones and other constituents of Vernonia spe- Adeboye, O.D., Ajayi, S.A., Baidu-Forson, J.J. & Opabode, cies from Ethiopia. Phytochemistry 37: 191–196. J.T. 2005. Seed constraint to cultivation and productivity of Abosi, A.O. & Raseroka, B.H. 2003. In vivo antimalarial ac- African indigenous leaf vegetables. African Journal of Bio tech- tivity of Vernonia amygdalina. British Journal of Biomedical Science nology 4: 1480–1484. 60: 89–91. Adylov, T.A. & Zuckerwanik, T.I. (eds.). 1993. Opredelitel Abrahamson, W.G., Blair, C.P., Eubanks, M.D. & More- rasteniy Srednei Azii, vol. 10. Conspectus fl orae Asiae Mediae, vol. head, S.A. 2003. Sequential radiation of unrelated organ- 10. Isdatelstvo Fan Respubliki Uzbekistan, Tashkent. isms: the gall fl y Eurosta solidaginis and the tumbling fl ower Afolayan, A.J. 2003. Extracts from the shoots of Arctotis arcto- beetle Mordellistena convicta.