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Comparative Genomics and Trait Evolution in Cleomaceae, a Model Family for Ancient Polyploidy

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Comparative Genomics and Trait Evolution in Cleomaceae, a Model Family for Ancient Polyploidy Comparative Genomics and Trait Evolution in Cleomaceae, a Model Family for Ancient Polyploidy Erik van den Bergh Propositions 1. To enjoy the evolutionary playground of polyploidy the hurdle of diploidization must first be passed. (this thesis) 2. Cleomaceae species provide a case study for the effects of polyploidy on numerous traits, such as C4 photosynthesis, glucosinolates and many others. (this thesis) 3. The accessibility of open data is as important as its availability. 4. Fabricated ‘truths’ in spite of scientific observations and conclusions show a lack of understanding, not a lack of goodwill. 5. What brings people together is not a good speech, but a good listen. 6. Parenthood is about guiding the next generation and forgiving the last. Propositions belonging to the thesis entitled: “Comparative genomics and trait evolution in Cleomaceae, a model family for ancient polyploidy” Erik van den Bergh Wageningen, May 17th 2017 COMPARATIVE GENOMICS AND TRAIT EVOLUTION IN CLEOMACEAE, A MODEL FAMILY FOR ANCIENT POLYPLOIDY ERIK VAN DEN BERGH Thesis committee Promotors Prof. Dr M.E. Schranz Professor of Biosystematics Wageningen University & Research Prof. Dr Y. van de Peer Professor in Bioinformatics and Genome Biology Ghent University, Belgium Other members Prof. Dr D. de Ridder, Wageningen University & Research Dr F.P. Lens, Naturalis, Leiden Dr M.G.M. Aarts, Wageningen University & Research Dr A.T. Groot, University of Amsterdam This research was conducted under the auspices of the Graduate School Experimental Plant Sciences COMPARATIVE GENOMICS AND TRAIT EVOLUTION IN CLEOMACEAE, A MODEL FAMILY FOR ANCIENT POLYPLOIDY Erik van den Bergh Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Wednesday 17 May 2017 at 1.30 p.m. in the Aula. Erik van den Bergh Comparative genomics and trait evolution in Cleomaceae, a model family for ancient polyploidy, 106 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2017) With references, with summaries in English and Dutch ISBN: 978-94-6343-170-5 DOI: http://dx.doi.org/10.18174/412208 CONTENTS Summary 6 Samenvatting 8 Introduction 10 Chapter 1 20 The genome of Tarenaya hassleriana provides insights into reproductive trait and genome evolution of crucifers Chapter 2 41 Gene and Genome Duplications and the Origin of C4 Photosynthesis: Birth of a Trait in the Cleomaceae Chapter 3 53 Flower power and the mustard bomb: Comparative analysis of gene and genome duplications in glucosinolate biosynthetic pathway evolution in Cleomaceae and Brassicaceae53 Chapter 4 67 Anthocyanins and flower colour in Cleome, identification of genetic variation underlying floral colouring patterns67 General Conclusion 81 References 84 Acknowledgements 103 SUMMARY As more and more species have been sequenced, evidence has been piling up for a fascinating phenomenon that seems to occur in all plant lineages: paleopolyploidy. Polyploidy has historically been a much observed and studied trait, but until recently it was assumed that polyploids were evolutionary dead-ends due to their sterility. However, many studies since the 1990’s have challenged this notion by finding evidence for ancient genome duplications in many genomes of current species. This lead to the observation that all seed plants share at least one ancestral polyploidy event. Another polyploidy event has been proven to lie at the base of all angiosperms, further signifying the notion that ancient polyploidy is widespread and common. These findings have led to questions regarding the apparent disadvantages that can be observed in a first generation polyploid. If these disadvantages can be overcome however, duplication of a genome also presents an enormous potential for evolutionary novelty. Duplicated copies of genes are able to acquire changes that can lead to specialization of the duplicated pair into two functions (subfunctionalization) or the development of one copy towards an entirely new function (neofunctionalization). Currently, most research towards polyploidy has focused on the economically and scientifically important Brassicaceae family containing the model plant Arabidopsis thaliana and many crops such as cabbage, rapeseed, broccoli and turnip. In this thesis, I lay the foundations for the expansion of this scope to the Cleomaceae, a widespread cosmopolitan plant family and a sister family of Brassicaceae. The species within Cleomaceae are diverse and exhibit many scientifically interesting traits. They are also in a perfect position phylogenetically to draw comparisons with the much more studied Brassicaceae. I describe the Cleomaceae and their relevance to polyploid research in more detail in the Introduction. I then describe the important first step towards setting up the genetic framework of this family with the sequencing of Tarenaya hassleriana in Chapter 1. In Chapter 2, I have studied the effects of polyploidy on the development of C4 photosynthesis by comparing the transcriptome of C3 photosynthesis based species Tarenaya hassleriana with the C4 based Gynandropsis gynandra. C4 photosynthesis is an elaboration of the more common C3 form of photosynthesis that concentrates CO2 in specific cells leading to decreased photorespiration by the RuBisCO and higher photosynthetic efficiency in low CO2 environments. I find that polyploidy has not led to sub- or neofunctionalization towards the development of this trait, but instead find evidence for another important phenomenon in postpolyploid evolution: the dosage balance hypothesis. This hypothesis states that genes which are dependent on specific dosage levels of their products will be maintained in duplicate; any change in their function would lead to dosage imbalance which would have deleterious effects on their pathway. We show that most genes involved in photosynthesis have returned to single copy in G. gynandra and that the changes leading to C4 have mostly taken place at the expression level confirming current assumptions on the development of this trait. In Chapter 3, I have studied the effects of polyploidy on an important class of plant defence compounds: glucosinolates. These compounds, sometimes referred to as ‘mustard oils’, play an important role in the defence against herbivores and have radiated widely in Brassicaceae to form many different ‘flavors’ to deter specific herbivores. I show that in Cleomaceae many genes responsible for these compounds have benefited from the three rounds of polyploidy that T. hassleriana has undergone and that many duplicated genes have been retained. We also show that more than 75% is actively expressed in the plant, proving that the majority of these duplications has an active function in the plant. Finally, in Chapter 4 I investigate a simple observation made during experiments with T. hassleriana in the greenhouse regarding the variation in flower colour between different individuals: some had pink flowers and some purple. Using LC-PDA mass spectrometry we find that the two colours are caused by different levels of two anthocyanin pigments, with cyanidin dominating in the purple flowers and 6 pelargonidin being more abundant in pink flowers. Through sequence comparison and synteny analysis between A. thaliana and T. hassleriana we find the orthologs of the genes involved in this pathway. Using a Genotyping by Sequencing method on a cross between these two flower colours, we produce a collection of SNP markers on the reference genome. With these SNPs, we find two significant binary trait loci, one of which corresponds to the location of the F3’H ortholog which performs the conversion of a pelargonidin precursor to a cyanidin precursor. In the General Conclusion, I combine all findings of the previous chapters and explain how they establish part of a larger species framework to study ancient polyploidy in angiosperms. I then put forth what these findings can mean for possible future research and the directions that are worth to be explored further. 7 SAMENVATTING Naarmate meer en meer soorten gesequenced worden, stapelt het bewijs zich op voor een fascinerend fenomeen dat lijkt voor te komen in alle plantenfamilies: paleopolyploïdie. Polyploïdie is historisch gezien een veel geobserveerde en bestudeerde eigenschap, maar tot recentelijk was de aanname dat polyploïden evolutionair gezien doodlopende lijnen waren vanwege hun steriliteit. Echter, veel studies sinds de jaren ’90 hebben deze aanname betwist met het vinden van bewijs voor zeer oude genoomduplicaties in vele genomen van huidige soorten. Dit heeft geleid tot de observatie dat alle zaadplanten op zijn minst één voorouderlijke polyploïdieronde delen. Daarbovenop is bewezen dat er een tweede polyploïdie aan de basis ligt van alle angiospermen, wat aannemelijk maakt dat voorouderlijke polyploïdie wijdverspreid en algemeen is. Deze vindingen leiden ook tot vragen over de ogenschijnlijke nadelen die geobserveerd kunnen worden in de eerste generatie van polyploïde organismen. Als deze nadelen echter kunnen worden overwonnen, leidt het dupliceren van het genoom tot een enorme hoeveelheid potentieel voor nieuwe evolutionaire mogelijkheden. Gedupliceerde kopieën van genen kunnen veranderingen verzamelen die kunnen leiden tot specialisatie van een genenpaar in twee nieuwe functies (subfunctionalisatie) of de ontwikkeling van één kopie tot een compleet nieuwe functie
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