Evolution and diversification of MADS-box genes following gene duplication

This PhD is focused around the deep evolutionary history of floral-organ identity MADS-box genes. MADS-box genes encode for transcription factors functioning in a diverse array of distinct processes throughout the development of flowering plants, from seed germination to seed set. This functional variation showcases their potential to diversify and evolve novel functions, making this gene family profoundly suitable to study the evolutionary forces that produced the awe-inspiring diversity of flowering plants. To that end, by studying their evolution and diversification around the time angiosperms originated, we provide a better understanding what role they played in the evolution of angiosperms or flowering plants. To do this, we utilize a multidisciplinary approach, which is a combination of phylogenetics, paleogenetics, modelling and experimental techniques.SUMMARY VII SAMENVATTING IX LIST OF ABBREVIATIONS XI TABLE OF CONTENTS XIII PREFACE 15 1. GENERAL INTRODUCTION 17 1.1. THE FLOWER 17 1.2. MADS-BOX TRANSCRIPTION FACTORS 20 1.3. DUPLICATION AND DIVERSIFICATION OF FLORAL GENES 27 1.4. GENETIC MODELS FOR THE EVOLUTION OF THE FLOWER 30 2. THE TANDEM ORIGIN OF ANGIOSPERM-SPECIFIC MADS-BOX GENES AND FLOWERING LOCUS C IN BRACHYPODIUM DISTACHYON. 35 2.1. INTRODUCTION 36 2.2. RESULTS 38 2.3. DISCUSSION 49 2.4. METHODS 52 2.5. ACKNOWLEDGEMENTS 57 3. WHEN PALEONTOLOGY AND MOLECULAR GENETICS MEET: A GENETIC CONTEXT FOR THE EVOLUTION OF CONIFER OVULIFEROUS SCALES 59 3.1. CONIFER OVULIFEROUS SCALES: AN EVOLUTION OF REDUCTION 60 3.2. GENETIC INSIGHTS INTO OVULIFEROUS SCALE DEVELOPMENT 61 4. A PRIMER ON THE USE OF PALEOGENETICS IN PLANT SCIENCES 65 4.1. BUILDING THE OLD FROM THE NEW 68 4.2. LEARNING FROM PREVIOUS PALEOGENETICS STUDIES 72 4.3. OPPORTUNITUES IN PLANT SCIENCES FOR A PALEOGENETICS APPROACH 75 4.4. BEYOND THE FUNDAMENTALS 83 5. THE ORIGIN OF FLORAL ORGAN IDENTITY QUARTETS 85 5.1. INTRODUCTION 86 5.2. RESULTS 89 5.3. DISCUSSION 103 5.4. METHODS 105 5.5. ACKNOWLEDGEMENTS 115 6. EMERGENCE OF MODULARITY IN SIMULATED EVOLUTION OF PROTEIN INTERACTION NETWORKS 117 6.1. INTRODUCTION 118 6.2. METHODS 121 6.3. RESULTS AND DISCUSSION 122 6.4. CONCLUSION AND OUTLOOK 129 7. GENERAL CONCLUSIONS AND FUTURE PROSPECTS 131 7.1. DUPLICATIONS IN THE EVOLUTION OF MIKCC MADS-BOX GENES 131 7.2. TOWARDS CLARIFYING DARWIN’S ABOMINABLE MYSTERY 134 7.3. MOLECULAR EVOLUTION OF PROTEIN-PROTEIN INTERACTIONS 136 8. SUPPLEMENTARY DATA 139 9. CURRICULUM VITAE 205 10. REFERENCES 209nrpages: 256status: publishe

When paleontology and molecular genetics meet: a genetic context for the evolution of conifer ovuliferous scales

published_online: 2013-08-26status: publishe

Choice of b-Lactam resistance pathway depends critically on initial antibiotic concentration

Antibiotic resistance trajectories with different final resistance may critically depend on the first mutation, due to epistatic interactions. Here, we study the effect of mutation bias and the concentration-dependent effects on fitness of two clinically important mutations in TEM-1 b-lactamase in initiating alternative trajectories to cefotaxime resistance. We show that at low cefotaxime concentrations, the R164S mutation (a mutation of arginine to serine at position 164), which confers relatively low resistance, is competitively superior to the G238S mutation, conferring higher resistance, thus highlighting a critical influence of antibiotic concentration on long-term resistance evolution

Supplementary material from "Interaction between mutation type and gene pleiotropy drives parallel evolution in the laboratory"

What causes evolution to be repeatable is a fundamental question in evolutionary biology. Pleiotropy, i.e. the effect of an allele on multiple traits, is thought to enhance repeatability by constraining the number of available beneficial mutations. Additionally, pleiotropy may promote repeatability by allowing large fitness benefits of single mutations via adaptive combinations of phenotypic effects. Yet, this latter evolutionary potential may be reaped solely by specific types of mutations able to realize optimal combinations of phenotypic effects while avoiding the costs of pleiotropy. Here, we address the interaction of gene pleiotropy and mutation type on evolutionary repeatability in a meta-analysis of experimental evolution studies with Escherichia coli. We hypothesize that single-nucleotide polymorphisms (SNPs) are principally able to yield large fitness benefits by targeting highly pleiotropic genes, whereas indels and structural variants (SVs) provide smaller benefits and are restricted to genes with lower pleiotropy. By using gene connectivity as proxy for pleiotropy, we show that non-disruptive SNPs in highly pleiotropic genes yield the largest fitness benefits, since they contribute more to parallel evolution, especially in large populations, than inactivating SNPs, indels and SVs. Our findings underscore the importance of considering genetic architecture together with mutation type for understanding evolutionary repeatability.This article is part of the theme issue ‘Predicting evolution’

The hybrid Four-CBS-Domain KINβγ subunit functions as the canonical γ subunit of the plant energy sensor SnRK1

The AMPK/SNF1/SnRK1 protein kinases are a family of ancient and highly conserved eukaryotic energy sensors that function as heterotrimeric complexes. These typically comprise catalytic α subunits and regulatory β and γ subunits, the latter function as the energy-sensing modules of animal AMPK through adenosine nucleotide binding. The ability to monitor accurately and adapt to changing environmental conditions and energy supply is essential for optimal plant growth and survival, but mechanistic insight in the plant SnRK1 function is still limited. In addition to a family of γ-like proteins, plants also encode a hybrid βγ protein that combines the Four-Cystathionine β-synthase (CBS)-domain (FCD) structure in γ subunits with a glycogen-binding domain (GBD), typically found in β subunits. We used integrated functional analyses by ectopic SnRK1 complex reconstitution, yeast mutant complementation, in-depth phylogenetic reconstruction, and a seedling starvation assay to show that only the hybrid KINβγ protein that recruited the GBD around the emergence of the green chloroplast-containing plants, acts as the canonical γ subunit required for heterotrimeric complex formation. Mutagenesis and truncation analysis further show that complex interaction in plant cells and γ subunit function in yeast depend on both a highly conserved FCD and a pre-CBS domain, but not the GBD. In addition to novel insight into canonical AMPK/SNF/SnRK1 γ subunit function, regulation and evolution, we provide a new classification of plant FCD genes as a convenient and reliable tool to predict regulatory partners for the SnRK1 energy sensor and novel FCD gene functions.status: publishe

Supplemental Data Set 8

Multiple alignment of SEP3/SEP1 used for ancestral protein reconstruction

Supplemental Data Set 2

Multiple alignment of AP3/PI used for estimating time of diversification

Supplemental Data Set 1

List of accessions of SEPALLATA-like, APETALA3- and PISTILLATA-like, AGAMOUS- and SEEDSTICK-like genes used for dating the E-class duplication

Data from: The origin of floral organ identity quartets

The origin of flowers has puzzled plant biologists ever since Darwin referred to their sudden appearance in the fossil record as an abominable mystery. Flowers are considered to be an assembly of protective, attractive and reproductive male and female leaf-like organs. Their origin cannot be understood by a morphological comparison to gymnosperms, their closest relatives, which develop separate male or female cones. Despite these morphological differences, gymnosperms and angiosperms possess a similar genetic toolbox consisting of phylogenetically related MADS-domain proteins. Using ancestral MADS-domain protein reconstruction, we trace the evolution of organ identity quartets along the stem lineage of crown angiosperms. We provide evidence that current floral quartets specifying male organ identity, which consist of four types of subunits, evolved from ancestral complexes of two types of subunits through gene duplication and integration of SEPALLATA proteins just before the origin of flowering plants. Our results suggest that protein interaction changes underlying this compositional shift were the result of a gradual and reversible evolutionary trajectory. Modelling shows that such compositional changes may have facilitated the evolution of the perfect, bisexual flower

Supplemental Data Set 7

Multiple alignment of AG/STK used for ancestral protein reconstruction