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Funktion Und Evolution Pflanzlicher B-Chromosomen

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Funktion Und Evolution Pflanzlicher B-Chromosomen Funktion und Evolution pflanzlicher B-Chromosomen Habilitationsschrift zur Erlangung des akademischen Grades doctor agriculturarum habilitatus (Dr. agr. habil.) verteidigt am 14.12.2009 an der Naturwissenschaftlichen Fakultät III der Martin-Luther-Universität Halle-Wittenberg von Dr. agr. Andreas Houben geb. am 06.05.1963 in Magdeburg Gutachter: Prof. Dr. Klaus Pillen (Martin-Luther Universität Halle-Wittenber) Prof. Dr. Thomas Schmidt (Technische Universität Dresden) Prof. Dr. Christian Jung (Christian-Albrechts-Universität zu Kiel) Dekan der Naturwissenschaftlichen Fakultät III Prof. Dr. Peter Wycisk Inhaltsverzeichnis Seite 1. Einleitung und Fragestellung 4 2. Eigene Arbeiten (A1-A20) 7 3. Zusammenfassende Diskussion 29 3.1. Ursprung und Evolution von B-Chromosomen 29 3.2. A- und B-Chromosomen können sich in der Verteilung 33 von Eu- und Heterochromatin-typischen Histonveränderungen unterscheiden 3.3. Meiotische B-Chromosomen zeigen eine veränderte 36 Zellzyklus-abhängige Histon H3-Phosphorylierung 3.4. Segregationsverhalten und Zentromere von 37 B-Chromosomen 3.5. B-Chromosomen zeigen eine schwache 39 Transkriptionsaktivität 3.6. Brachycome dichromosomatica, eine Modellart für die 40 Analyse von B-Chromosomen 3.7. Potentielle Anwendung von B-Chromosomen in der 43 Biotechnologie 4. Zusammenfassung (in Deutsch und Englisch) 44 5. Literaturverzeichnis 52 Danksagung 58 2 Abkürzungsverzeichnis bp Basenpaar Bs B-Chromosomen 2C DNA-Gehalt des diploiden, unreplizierten Chromosomensatzes DAPI 4’,6’-Diamidino-2-Phenylindol FISH Fluoreszenz-in-situ-Hybridisierung G1 Zellzyklusphase G1 G2 Zellzyklusphase G2 ITS2 Internal-Transcribed-Spacer 2 K4 Lysin 4 K9 Lysin 9 K20 Lysin 20 K27 Lysin 27 H3 Histon H3 H4 Histon H4 mB Mikro-B-Chromosomen Mbp Megabasenpaare me methyliert me1 monomethyliert me2 dimethyliert me3 trimethyliert nB Standard-B-Chromosomen NOR Nukleolusorganisatorregion rDNA ribosomale DNA rRNA ribosomale RNA PCR Polymerase-Kettenreaktion ph Phorphorylierung RT-PCR Reverse-Transcriptase-PCR S10 Serin 10 S28 Serin 28 T3 Threonin 3, T11 Threonin 11 T32 Threonin 32 3 1. Einleitung und Fragestellung Chromosomen portionieren das Genom und ermöglichen die korrekte Weitergabe der Zellkern-lokalisierten Erbinformation. Die Genomgröße und Anzahl der Chromosomen innerhalb einer Spezies sind weitgehend konstant. Häufig ist aber die Artenevolution mit einer numerischen und strukturellen Karyotypveränderung verbunden, wodurch sich die Genomgröße und Anzahl von Chromosomen einzelner Individuen einer Art unterscheiden kann. Eine Vielzahl von pflanzlichen und tierischen Arten besitzen neben den normalen Standardchromosomen oder auch A-Chromosomen genannt, überzählige sogenannte B-Chromosomen. Diese Zusatzchromosomen unterscheiden sich von den A-Chromosomen dadurch, dass diese keine essentiellen Erbinformationen besitzen, ein nicht-mendelndes Segregationsverhalten zeigen und auch nicht mit den A-Chromosomen während der Meiose paaren (Jones and Rees, 1982; Jones, 1991a; Jones and Puertas, 1993; Beukeboom, 1994; Jones, 1993; Bougourd and Jones, 1997; Covert, 1998; Camacho et al., 2000; Puertas, 2002; Jones et al., 2008). Sie treten gewöhnlich nur in einigen Individuen einer Art auf (Jones, 2004). Außerdem kann ihre Anzahl innerhalb und zwischen Individuen variieren. B- Chromosomen können extrem hohe Zahlen in natürlichen Populationen erreichen, abhängig davon, wie viele zusätzliche Chromosomen eine bestimmte Art tolerieren kann (Camacho et al., 2000). Durch diese unikalen Eigenschaften kann sich die Evolution beider Chromosomentypen unterscheiden. Da in der überwiegenden Mehrzahl die Gegenwart von B-Chromosomen, vor allem in höherer Kopienzahl, sich negativ auf die Vitalität und Fruchtbarkeit des Trägerorganismus auswirken kann, werden B-Chromosomen oftmals als parasitäre Bestandteile des Genoms eingestuft. Die Verteilung von B-Chromosomen innerhalb der Angiospermen ist nicht zufällig. Fremdbefruchtende Arten mit großen Genomen und wenigen Chromosomen besitzen bevorzugt diesen Chromosomentyp. Die Auswertung der B-Chromosomen- Verteilung zeigte auch, dass B-Chromosomen gleich oft in polyploiden und diploiden Arten auftreten (Palestis et al., 2004; Trivers et al., 2004; Levin et al., 2005). Die positive Korrelation zwischen Genomgröße und der Gegenwart von B- Chromosomen kann evtl. dadurch erklärt werden, dass großgenomige Arten 4 zusätzliche Chromosomen leichter tolerieren können (Puertas, 2002) oder, da das Genom großgenomiger Arten hauptsächlich aus nicht-kodierender DNA besteht, diese Genomkomponente die Formierung von B-Chromosomen unterstützt (Levin et al., 2005). Die Auswertung von 23.652 Angiospermen (rund 9% der geschätzten 260.000 Arten) zeigte, dass zirka 8% der Monokotyledonen und 3% der Eudicots Träger von B-Chromosomen sind. In den besonders artenreichen Poaceae und Asteraceae wurden am häufigsten Zusatzchromosomen nachgewiesen. Dagegen besitzen Liliales und Commelinales besonders viele Arten mit B-Chromosomen (Palestis et al., 2004; Levin et al., 2005). Obwohl seit der Erstbeschreibung von B-Chromosomen durch Wilson (1907) die rätselhaften Eigenschaften dieser Genomkomponente das Interesse einer Vielzahl von Forschern geweckt haben, sind noch viele Fragen zur Evolution und Funktionsweise von B-Chromosomen unbeantwortet. Insgesamt liegen dieser Habilitationsarbeit 20 Originalarbeiten zugrunde. Ziel meiner Arbeit war es: (A) den Ursprung und die Evolution von B-Chromosomen zu erkunden; (B) die Chromatinzusammensetzung von A- und B-Chromosomen zu vergleichen und chromosomale Verteilung von Eu- und Heterochromatin-typischen Histonveränderungen zu bestimmen. (C) B-Chromosomen zur Funktionsbestimmung von Zellzyklus-abhängigen Histon H3 Phosphorylierungen einzusetzen. (D) die Transkriptionsaktivität, der sogenannten „genetisch inaktiven“ B- Chromosomen erstmals molekulargenetisch zu charakterisieren. (E) Brachycome dichromosomatica als Modellart für die Analyse von B- Chromosomen zu etablieren. Zur Bearbeitung der aufgelisteten Themen wurden von mir bevorzugt B- Chromosomen des Roggens (Secale cereale L., 2n= 14 +0-8 Bs), der Australischen 5 Gänseblume (Brachycome dichromosomatica, Synonym: Brachyscome dichromosomatica, 2n= 4 +0-3 Standard Bs + 0-9 Mikro Bs), der Puschkinie (Puschkinia libanotica, 2n= ? + 0-7 Bs), und des Kleinköpfigen Pippau (Crepis capillaris, 2n= 6 +0-4 Bs) experimentell untersucht. Die B-Chromosomen des Roggens wurden untersucht, da bereits viele Vorarbeiten an diesen Chromosomen durchgeführt worden waren (Jones und Puertas, 1993) und somit die DNA-Zusammensetzung der Roggen Bs teilweise bekannt war. Aufgrund der geringen A-Chromosomenanzahl (2n = 4) und der Existenz von zwei B- Chromosomentypen war B. dichromosomatica prädestiniert, um die Evolution, DNA und Chromatinzusammensetzung von Bs zu erkunden. C. capillaris wurde ausgewählt, da diese Art B-lokalisierte rDNA Sequenzen besitzt, welche zur Analyse der Transkription und Phylogenie von B-Chromosomen geeignet sind. 6 2. Eigene Arbeiten (A1-A20) A1 Carchilan, M., Delgado, M., Ribeiro, T., Costa-Nunes, P., Caperta, A., Morais- Cecilio, L., Jones, R.N., Viegas, W., and Houben, A. (2007). Transcriptionally active heterochromatin in rye B chromosomes. Plant Cell 19, 1738-1749. A2 Cohen, S., Houben, A., and Segal, D. (2008). Extrachromosomal circular DNA derived from tandemly repeated genomic sequences in plants. Plant Journal 53, 1027-1034. A3 Gernand, D., Demidov, D., and Houben, A. (2003). The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet Genome Res 101, 172-176. A4 Gernand, D., Rutten, T., Varshney, A., Rubtsova, M., Prodanovic, S., Bruss, C., Kumlehn, J., Matzk, F., and Houben, A. (2005). Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. Plant Cell 17, 2431-2438. A5 Houben, A., and Schubert, I. (2007). Engineered plant minichromosomes: a resurrection of B chromosomes? Plant Cell 19, 2323-2327. A6 Houben, A., Demidov, D., Caperta, A.D., Karimi, R., Agueci, F., and Vlasenko, L. (2007). Phosphorylation of histone H3 in plants - A dynamic affair. Biochim Biophys Acta. A7 Houben, A., Demidov, D., Rutten, T., and Scheidtmann, K.H. (2005). Novel phosphorylation of histone H3 at threonine 11 that temporally correlates with condensation of mitotic and meiotic chromosomes in plant cells. Cytogenet Genome Res 109, 148-155. A8 Houben, A., Demidov, D., Gernand, D., Meister, A., Leach, C.R., and Schubert, I. (2003). Methylation of histone H3 in euchromatin of plant chromosomes depends on basic nuclear DNA content. Plant Journal 33, 967- 973. A9 Houben, A., Verlin, D., Leach, C.R., and Timmis, J.N. (2001). The genomic complexity of micro B chromosomes of Brachycome dichromosomatica. Chromosoma 110, 451-459. 7 A10 Houben, A., Wanner, G., Hanson, L., Verlin, D., Leach, C.R., and Timmis, J.N. (2000). Cloning and characterisation of polymorphic heterochromatic segments of Brachycome dichromosomatica. Chromosoma 109, 433-433. A11 Houben, A., Thompson, N., Ahne, R., Leach, C.R., Verlin, D., and Timmis, J.N. (1999). A monophyletic origin of the B chromosomes of Brachycome dichromosomatica (Asteraceae). Plant Syst Evol 219, 127-135. A12 Houben, A., Belyaev, N.D., Leach, C.R., and Timmis, J.N. (1997a). Differences of histone H4 acetylation and replication timing between A and B chromosomes of Brachycome dichromosomatica.
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