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Downloaded from Genbank THE MOLECULAR EVOLUTION OF FLORAL COLOUR SHIFTS IN LATHYRUS L. (FABACEAE) by Xinxin Xue M.Sc., The University of Edinburgh, 2008 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) December 2015 © Xinxin Xue, 2015 Abstract In this thesis, I used Lathyrus to study floral colour evolution. My work builds on that of pioneer geneticists who used the sweet pea (Lathyrus odoratus) for research in early 20th century England. They used the rich horticultural resource of inbred cultivars for genetic study. More recently, studies on flavonoid biochemistry and the phylogenetics of Lathyrus lend tools to place the colour shifts in an evolutionary and molecular context. In chapter 2, I show that the A1 locus is a missense mutation (332 G/A) in the substrate recognition site (SRS1) of flavonoid 3’,5’-hydroxylase (F3’5’H) and is associated with the pink mutant cultivar ‘Painted Lady’ (‘PL’). This single base pair substitution in the mutant F3’5’H is speculated to toggle the enzyme from primary F3’5’H activity to a relatively efficient F3’H, as shown in a heterologous transformation in Arabidopsis PAP1D (a mutant line that produces anthocyanin constitutively). In chapter 3, I constructed a multi-species coalescent tree using Bayesian inference and reconstructed the ancestral states for floral colour, life history trait (perennial or annual) and floral pattern. The ancestral states for Lathyrus are anthocyanin rich (AR), annual and concolourous. However, no correlation was found between the life history trait (which is linked to breeding systems) and the loss of anthocyanin colour in the petal, when corrected for phylogenetic independence. This suggests that in Lathyrus, autogamous species are as colourful as allogamous ones even though the latter are expected to need greater floral display. In chapter 4, I found that the lack of expression in dihydroflavonol reductase (DFR) was associated with a white mutant cultivar ‘Mrs Collier’ (‘MC’) of L. odoratus via a trans-regulatory machinery. Two transcription factors, the sweet pea orthologues of AN2 (MYB) and AN1 (bHLH) were also not expressed although neither was associated with the white phenotype in an F2-cosegregation analysis. This DFR silencing was also observed in another white mutant of the domesticated grass pea (L. sativus). In contrast, when unpigmented wild species originate under natural selection, DFR expression, if at all affected, is lowered rather than fully silenced, likely due to pleiotropic effects. ii Preface This thesis represents original unpublished work by Xinxin Xue, with inputs from others as stated in the text and here. All chapters will be prepared for publication. Chapter 2 I designed and carried out all the experiments and data analysis with inputs from others. Quentin Cronk provided the idea, performed the crosses and supplied F2 seed. Lina Madilao at the Bohlmann lab carried out the LC analysis. Meixuezi Tong from the Li lab assisted with Arabidopsis transformation. Saemundur Sveinsson analyzed the transcriptomic data. Chapter 3 I designed and carried out all the analysis. Most of the DNA sequence data was downloaded from GenBank. Chapter 4 I designed the study with input from Quentin Cronk who performed the crosses and supplied F2 seed. I carried out all the experiments and data analysis. Lina Madilao operated the LC-MS analysis. iii Table of Contents Abstract ................................................................................................................................... ii Preface .................................................................................................................................... iii Table of Contents ................................................................................................................... iv List of Tables ......................................................................................................................... vii List of Figures ...................................................................................................................... viii List of Abbreviations ............................................................................................................... x Acknowledgements ................................................................................................................ xi Chapter 1. Introduction .......................................................................................................... 1 1.1 Overview of flower colour shifts in an evolutionary context .......................................... 1 1.2 Biochemistry of flower colour ......................................................................................... 2 1.3 Introducing the system: Lathyrus .................................................................................... 3 1.4 Objective of the thesis ...................................................................................................... 4 Chapter 2. The Molecular Basis for a Pink Mutant in Sweet Pea ...................................... 5 2.1 Introduction ...................................................................................................................... 5 2.2 Materials and methods ..................................................................................................... 7 2.2.1 Plant materials and crossing ...................................................................................... 7 2.2.2 Pigment analysis ........................................................................................................ 7 2.2.3 Extraction of nucleic acid, cDNA synthesis and PCR .............................................. 8 2.2.4 F2 co-segregation analysis ........................................................................................ 9 2.2.5 Binary vector construction, transformation into Arabidopsis thaliana .................... 9 2.3 Results ............................................................................................................................ 10 2.3.1 The pink mutant ‘PL’ lacks delphinidin derivatives, but produces more cyanidin 10 2.3.2 A missense mutation in F3’5’H is associated with the pink colour in ‘PL’ ........... 10 2.3.3 Elevated production of cyanidin in the ‘PL’ F3’5’H-transformed Arabidopsis PAP1- D line ................................................................................................................................ 11 2.4 Discussion ...................................................................................................................... 12 2.4.1 A missense mutation in ‘PL’ F3’5’H occurred at a structurally critical site .......... 12 2.4.2 Overexpression of sweet pea wild type F3’5’H increases the accumulation of cyanidin in Arabidopsis .................................................................................................... 13 2.4.3 Overexpression of sweet pea F3’5’H in Arabidopsis PAP1D failed to accumulate iv delphinidin ........................................................................................................................ 14 2.4.4 Alteration of the SRS1 domain of sweet pea F3’5’H greatly increased the accumulation of cyanidin in a heterologous system ........................................................ 15 2.4.5 Evolutionary implications ....................................................................................... 17 Chapter 3. Phylogenetic Reconstruction for Floral Colour, Life History Trait and Pattern in Lathyrus ................................................................................................................ 24 3.1 Introduction .................................................................................................................... 24 3.2 Materials and methods ................................................................................................... 25 3.2.1 Data collection and taxon sampling ........................................................................ 25 3.2.2 Phylogenetic reconstruction of Lathyrus ................................................................ 26 3.2.3 Ancestral reconstruction of floral traits and correlation analysis ........................... 26 3.2.4 UV photography ...................................................................................................... 27 3.3 Results ............................................................................................................................ 28 3.3.1 Main phylogenetic results ....................................................................................... 28 3.3.2 Ancestral reconstruction and correlation analysis .................................................. 29 3.4 Discussion ...................................................................................................................... 30 3.4.1 Justification for ancestral reconstruction based on BEAST tree ............................ 30 3.4.2 Lack of association between anthocyanin-pigmented form and life history .......... 31 3.4.3 Polarity of trait evolution ........................................................................................ 32 3.4.4 Spectral limitation of this study .............................................................................. 33 Chapter 4. The Genetic Basis for Parallel Evolution of ‘White Shifts’ in Lathyrus ....... 46 4.1
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