Understanding Flowers and Flowering: An Intergrated Approach

251 Pages·2008·2.52 MB·English

by  Beverly Glover

Understanding
Flowers
& Flowering
An Integrated Approach
Understanding Flowers and Flowering
This page intentionally left blank
Understanding
Flowers and
Flowering
An Integrated Approach
Beverley J. Glover
1
3
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ISBN 978–0–19–856597–0 978–0–19–856596–3 (pbk.)
10 9 8 7 6 5 4 3 2 1
Preface
Flowers are the features of plants that most endear to provide students and researchers studying one
them to human beings. We grow flowers in our gar- aspect of floral biology with an overview of other
dens, we display them in our homes, and they fea- important aspects of flowers, both to help them to
ture prominently in our artistic history. Scientists, set their own work in context and to encourage
too, have been fascinated by flowers, and there is a them to consider experiments which might lead to
long tradition of botanical study of floral structure greater integration of the field. In particular, I hope
and floral ecology. However, it is only recently that that this book will encourage dialogue between flo-
the tools of molecular genetics have been applied to ral biologists of all varieties, with a long-term view
flower induction, development, and morphology. to ensuring a continuing increase in interdiscipli-
The data arising from these studies, when com- nary studies.
bined with painstaking observation and analysis of The book is divided into three main sections.
the interactions of plants with their pollinators, are Section I is introductory, giving some necessary
beginning to provide the first truly integrated background to the evolution of flowers and to the
understanding of both how and why flowers take history of scientific thought on flowers and flower-
the forms we so admire. ing. Section II considers the molecular mechanisms
Traditionally, flowers are studied from one of a that control flower induction, flower development,
number of viewpoints. Molecular biologists may and floral mating type, providing coverage of the
study the genetic control of flower induction or genetic material available for shaping by natural
flower development, usually focusing on one, or a selection. This section is initially focused on a very
very small number of, model species. Evolutionary few species of model plants, looking at the molecu-
biologists may study how flowers evolved, the lar similarities which unite all flowers. In the later
forms of the earliest flowers, or the development of chapters it considers the development and repro-
flowers of ancient lineages alive today. Pollination ductive strategies of plants from a range of species.
biologists may study the interactions between Section III extends this analysis much further, con-
plants and their pollinating animals, the natural sidering the explanations for the differences
selection exerted by those pollinators, and how between flowers, rather than their similarities. This
these pressures affect plant population dynamics. section moves between molecular explanations for
However, it is becoming clear that these various flower morphology and the ecological conse-
disciplines each have enormous power to inform quences of that morphology, in an attempt to inte-
and shape the work of the others. An understand- grate what we know both of how and why different
ing of how flower colour is controlled biochemi- flowers take their different forms. Finally, the epi-
cally and genetically, for example, can be of great logue attempts to draw out some themes which
benefit when studying how pollinator-imposed persist throughout the book, suggesting possible
selection might have influenced the evolution of future directions for the field.
petal colour within a group of plants. Many people have contributed to the final shape
I hope that this book might serve as a starting of this book, and I am particularly grateful to mem-
point for those interested in taking such an inte- bers of my own research laboratory for enthusiastic
grated approach to the study of flowers. My aim is support and helpful discussions at many points in
v
vi PREFACE
the process. John Parker, Caroline Dean, David for the line drawings. Thanks also to Roy Barlow
Hanke, Cathie Martin, Jeff Ollerton, Rob Raguso, and Don Manning for their excellent cover design.
and Nick Waser read various sections in detail, and At Oxford University Press, Ian Sherman has
I must thank them all for the time and care that provided steadfast support for this project, dealing
they took and for their excellent suggestions and with various changes to the schedule with calm
advice. Many people were kind enough to provide good humour while Helen Eaton and Christine Rode
me with images for figures. While these are have kindly shepherded me through the production
acknowledged in the relevant figure legends, I par- process. On a personal note I must thank Jocelyn,
ticularly thank Nick Waser, Enrico Coen, and the Duncan, and Katie Taylor for lending me the space
Cambridge University Botanic Garden for their great and quiet to really begin writing, rather than just
generosity in sharing images, Kit Wilkins for help thinking about it. Finally, I thank my parents for
with graphics packages, Matthew Dorling and their endless encouragement, and Stuart, David,
Heather Whitney for photographic assistance, Mike Rosie, and Sam, who put up with me during this
Webb for biochemical pathways, and Rosie Bridge process with remarkable patience and love.
Contents
Preface v
SECTION I INTRODUCTION 1
1 The Evolution of Flowers 3
1.1 The origin of flowering plants 3
1.2 Early reproductive structures 7
1.3 The first flowers 7
1.4 Floral diversification 8
2 Historical Interpretations of Flower Induction and Flower Development 10
2.1 The foliar theory of the flower 10
2.2 The foliar theory in an evolutionary context 15
2.3 The transition to flowering 15
2.4 Developmental explanations of floral induction 16
2.5 Environmental explanations of floral induction 16
2.6 The florigen problem 19
SECTION II THE MOLECULAR MECHANISMS OF FLOWERING:INDUCTION
AND DEVELOPMENT 21
PART A Induction of Flowering 23
3 Flower Induction in Arabidopsis thaliana 25
3.1 Arabidopsis thalianaas a model system for the study of flowering 25
3.2 Flowering-time mutants 30
4 The Autonomous Pathways for Floral Inhibition and Induction 35
4.1 The floral inhibition pathway 35
4.2 The autonomous induction pathway 39
4.3 Other endogenous factors which influence flowering time 41
5 The Photoperiodic Pathway of Floral Induction 43
5.1 Sensing daylight 43
5.2 Measuring time 48
5.3 Integrating light and clock signals 50
6 The Vernalization Pathway of Floral Induction and the Role of Gibberellin 52
6.1 The vernalization promotion pathway 52
vii
viii CONTENTS
6.2 The gibberellin promotion pathway 56
6.3 Does gibberellin act in the vernalization promotion pathway as
well as independently? 58
7 Integrating the Arabidopsis thalianaFlower Induction Pathways and
Assessing the Extent to Which the Model Is Ubiquitous 59
7.1 Integrating the flowering-time pathways 59
7.2 The Arabidopsis flowering-time model in other species 64
PART B Development of Flowers 69
8 Changes at the Shoot Apical Meristem in Response to Floral Induction 71
8.1 Physiological changes at the shoot apical meristem 71
8.2 Shoot apical meristem anatomy 72
8.3 Gene expression patterns in the shoot apical meristem 73
8.4 Floral meristem identity genes act downstream of the
flowering-time integrators 74
8.5 Floral meristem identity genes 74
9 Development of the Floral Organs 83
9.1 The original ABC model of flower development 83
9.2 The role of D function genes 90
9.3 The role of E function genes 90
9.4 The role of cadastral genes 92
9.5 The quartet model of organ identity 94
10 The ABC Model in Evolution 95
10.1 Evolutionary history of MADS box transcription factors 95
10.2 ABC model in gymnosperms? 96
10.3 ABC model in monocots? 98
10.4 Variations on the ABC model 101
11 Function and Development of Gametophytes 103
11.1 Alternation of generations in multicellular organisms 103
11.2 The angiosperm female gametophyte 105
11.3 The angiosperm male gametophyte 107
11.4 Events following pollination 109
12 Preventing Self-fertilization 111
12.1 Reducing self-pollination in a hermaphroditic flower 111
12.2 Monoecy 113
12.3 Dioecy 114
12.4 Self-incompatibility (SI) 115
12.5 Sporophytic self-incompatibility (SSI) 116
12.6 Gametophytic self-incompatibility (GSI) 119
12.7 Heteromorphic self-incompatibility 120
CONTENTS ix
SECTION III POLLINATION SUCCESS:MOLECULAR AND ECOLOGICAL INTERACTIONS 123
PART A How and Why Does Floral Form Vary? 125
13 Why Are Flowers Different? Pollination Syndromes—The Theory 127
13.1 Cross pollination 127
13.2 Abiotic pollen vectors 127
13.3 Biotic pollen vectors 129
13.4 Principles underlying the pollination syndrome concept 129
13.5 The pollination syndromes 130
14 Changing Floral Shape and Structure 138
14.1 Changing corolla size 138
14.2 Changing corolla symmetry 140
14.3 Changing petal shape 143
14.4 Generating a composite inflorescence 145
15 Colouring the Flower 147
15.1 Colour as a signal 147
15.2 Plant pigments 148
15.3 Carotenoid synthesis 149
15.4 Flavonoid synthesis 151
15.5 Betalains 156
16 Enhancing Flower Colour 158
16.1 Mixing pigments 158
16.2 Co-pigmentation 158
16.3 Regulation of pigment distribution 159
16.4 The effects of metal ions 162
16.5 The importance of pH 163
16.6 The role of petal cell shape 165
PART B The Influence of Pollinators on Floral Form 169
17 Are Flowers under Selective Pressure to Increase Pollinator Attention? 171
17.1 Competition for pollinator attention 171
17.2 Facilitation of pollination 172
17.3 Techniques for investigating the role of pollinator attention in
limiting fitness 172
17.4 Evidence based on fruit and seed set following hand pollination 175
17.5 Evidence from mixed species plots 176
17.6 Analysis of character traits potentially displaced by pollination
competition 177
18 Do Pollinators Discriminate between Different Floral Forms? 181
18.1 What pollinators see 181
18.2 What pollinators sense in other ways 183
18.3 Discrimination between petals of different colours 184