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Evolution of the Interaction of Floral Homeotic Proteins

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Evolution of the Interaction of Floral Homeotic Proteins Evolution of the interaction of floral homeotic proteins Dissertation Zur Erlangung des akademischen Grades ‘doctor rerum naturalium‘ (Dr. rer. nat.) Vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät der Friedrich-Schiller-Universität Jena von Diplombiologe Florian Rümpler geboren am 04. Dezember 1986 in Erfurt Gutachter 1. Prof. Dr. Günter Theißen (Jena) 2. Asst. Prof. Dr. Rainer Melzer (Dublin) 3. Prof. Dr. Richard Immink (Wageningen) Tag der öffentlichen Verteidigung Mittwoch 15. November 2017 Table of contents 1 Introduction ............................................................................................................................... 3 1.1 MADS-domain transcription factors in plants - a K-domain blessing .............................. 3 1.2 MIKCC-type MADS-TFs controlling flower development of angiosperms ..................... 6 1.3 The protein-protein interaction network of floral homeotic proteins ................................ 8 1.4 The keratin-like domain of MIKCC-type proteins ............................................................. 9 1.5 Floral homeotic proteins as targets of plant pathogen effectors ...................................... 11 1.6 Aims of this thesis ........................................................................................................... 14 2 Manuscripts ............................................................................................................................. 15 2.1 Manuscript overview ....................................................................................................... 15 2.2 Manuscript I ..................................................................................................................... 20 Melzer, R., Härter, A., Rümpler, F., Kim, S., Soltis, P. S., Soltis, D. E., Theißen, G. (2014). DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution. Ann. Bot. 114, 1431-1443. 2.3 Manuscript II ................................................................................................................... 34 Rümpler, F., Theißen, G., Melzer, R. (2015). Character-state reconstruction to infer ancestral protein-protein interaction patterns. Bio-protocol 5, published online. 2.4 Manuscript III .................................................................................................................. 45 Rümpler, F., Gramzow, L., Theißen, G., Melzer, R. (2015). Did convergent protein evolution enable phytoplasmas to generate 'zombie plants'? Trends Plant Sci. 20, 798-806. 2.5 Manuscript IV .................................................................................................................. 55 Theißen, G., Melzer, R., Rümpler, F. (2016). MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143, 3259-3271. 2.6 Manuscript V ................................................................................................................... 69 Rümpler, F., Theißen, G., Melzer, R. (2017). Sequence features of MADS-domain proteins that act as hubs in the protein-protein interaction network controlling flower development. bioRxiv,125294. 3 Discussion ............................................................................................................................... 98 3.1 Evolution of the PPI network controlling flower development of angiosperms ............. 98 3.2 Origin and evolution of floral quartet-like complex formation ..................................... 101 3.3 Sequence features determining protein-protein interactions of floral homeotic proteins ......... 103 3.4 Implications of the K-domain mimicry of SAP54 ......................................................... 107 4 Summary ............................................................................................................................... 109 4.1 Summary ........................................................................................................................ 109 4.2 Zusammenfassung ......................................................................................................... 110 5 Bibliography ......................................................................................................................... 111 6 Acknowledgements ............................................................................................................... 129 7 Declaration of authorship (Ehrenwörtliche Erklärung) ........................................................ 130 8 Curriculum vitae ................................................................................................................... 131 9 Publications and conference contributions ........................................................................... 132 Introduction 1 Introduction Developmental processes are controlled by the dynamic interplay between transcription factors and their target genes. Thereby transcription factors often bind to DNA not as monomers but as higher order homo- and heteromeric complexes. The activation or repression of target genes therefore highly depends on the protein-protein interactions of the corresponding transcription factor. A good case in point are floral homeotic MADS-domain transcription factors (MADS-TFs) that bind as heterotetramers to cis-regulatory DNA elements of target genes to control floral organ identity determination of angiosperms (Theißen and Saedler, 2001). It is presumed that the composition of the heterotetramer determines the set of target genes and eventually defines the identity of the developing floral organ. The protein-protein interactions of floral homeotic MADS-TFs and the structure and evolution of the protein-protein interaction network (PPI network) controlling flower development are thus of great scientific interest. With this thesis I aim to deepen our understanding of the molecular mechanisms underlying the protein-protein interactions of floral homeotic MADS-TFs and to give insights into how certain interaction patterns of floral homeotic proteins changed in the course of angiosperm evolution. 1.1 MADS-domain transcription factors in plants - a K-domain blessing MADS-box genes are a synapomorphy of eukaryotes and encode for MADS-TFs that control a variety of different developmental processes of animals, plants and fungi (Messenguy and Dubois, 2003). Whereas only few MADS-box genes are present in animals and fungi (Messenguy and Dubois, 2003), their number dramatically increased during plant evolution, with more than 100 gene family members being present in Arabidopsis thaliana (Parenicova et al., 2003; Gramzow and Theißen, 2010). All MADS-TFs share a highly conserved DNA-binding MADS-domain, with ‘MADS’ being an acronym for the four founding members of this protein family: MINICHROMOSOME MAINTENANCE FACTOR 1, AGAMOUS, DEFICIENS, and SERUM RESPONSE FACTOR (Schwarz-Sommer et al., 1990). An ancestral gene duplication in the stem group of extant eukaryotes gave rise to two clades of MADS-box genes, termed Type I and Type II genes (Alvarez-Buylla et al., 2000; Gramzow et al., 2010). Whereas relatively little is known about function and evolution of Type I MADS-box genes in plants, Type II genes constitute key regulators of many developmental processes in angiosperms and they are therefore 3 Introduction one of the best studied gene families within plants (Kaufmann et al., 2005a; Gramzow and Theißen, 2010; Smaczniak et al., 2012a; Gramzow and Theißen, 2013). Plant Type II MADS-TFs are characterized by a conserved domain structure comprising the highly conserved MADS-domain (M), followed by an intervening (I), a keratin-like (K) and a C-terminal (C) domain (Theißen et al., 1996; Becker and Theißen, 2003; Kaufmann et al., 2005a). This conserved architecture is unique to plant Type II MADS-TFs and due to this domain structure plant Type II MADS-TFs are also referred to as MIKC-type proteins. Whereas MADS- and I-domain function in the formation of DNA-bound dimers, the K-domain enables (at least many) MIKC-type proteins to also tetramerize among each other (Melzer and Theißen, 2009; Melzer et al., 2009; Smaczniak et al., 2012b; Puranik et al., 2014). It is presumed that the emergence of the K-domain was a key event in the evolution of plant Type II MADS-TFs and that the conjunction of a DNA-binding MADS-domain with a protein-protein interaction domain was of importance for success of this transcription factor family (Kaufmann et al., 2005a; Manuscript IV: Theißen et al., 2016; Manuscript V: Rümpler et al., 2017). MIKC-type genes are found in charophytes (freshwater green algae) but not in chlorophytes (Tanabe et al., 2005; Derelle et al., 2006). Thus it appears most likely that the recruitment of the K-domain took place in the stem group of extant streptophytes (charophytes and land plants) (Fig. 1). During streptophyte evolution MIKC-type genes further diverged into two groups: MIKCC and MIKC* (Fig. 1) (Henschel et al., 2002; Kaufmann et al., 2005a; Gramzow and Theißen, 2010). In angiosperms MIKCC-type genes predominantly function in sporophyte development, whereas the expression of MIKC*-type genes is mainly restricted to the male gametophyte (Zobell et al., 2010; Kwantes et al., 2012; Smaczniak et al., 2012a). Structurally MIKCC- and MIKC*-type genes differ in length and number of the exons that encode for the K-domain (Henschel et al., 2002; Kwantes et al., 2012). It is not entirely clear as to exactly when the duplication
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