Flowering and its Manipulation Edited by CHARLES AINSWORTH Department of Agricultural Sciences Imperial College Wye Campus Ashford Kent UK Flowering and its Manipulation Annual Plant Reviews A series for researchers and postgraduates in the plant sciences. Each volume in this series focuses on a theme of topical importance and emphasis is placed on rapid publication. Editorial Board: Professor Jeremy A. Roberts (Editor-in-Chief), Plant Science Division, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK; Dr David Evans, School of Biological and Molecular Sci- ences, Oxford Brookes University, Headington, Oxford, OX3 0BP; Professor Hidemasa Imaseki, Obata-Minami 2419, Moriyama-ku, Nagoya 463, Japan; Dr Michael T. McManus, Institute of Molecular BioSciences, Massey University, Palmerston North, New Zealand; Dr Jocelyn K.C. Rose, Department of Plant Biology, Cornell University, Ithaca, New York 14853, USA. Titles in the series: 1. Arabidopsis Edited by M. Anderson and J.A. Roberts 2. Biochemistry of Plant Secondary Metabolism Edited by M. Wink 3. Functions of Plant Secondary Metabolites and their Exploitation in Biotechnology Edited by M. Wink 4. Molecular Plant Pathology Edited by M. Dickinson and J. Beynon 5. Vacuolar Compartments Edited by D.G. Robinson and J.C. Rogers 6. Plant Reproduction Edited by S.D. O’Neill and J.A. Roberts 7. Protein–Protein Interactions in Plant Biology Edited by M.T. McManus, W.A. Laing and A.C. Allan 8. The Plant Cell Wall Edited by J.K.C. Rose 9. The Golgi Apparatus and the Plant Secretory Pathway Edited by D.G. Robinson 10. The Plant Cytoskeleton in Cell Differentiation and Development Edited by P.J. Hussey 11. Plant–Pathogen Interactions Edited by N.J. Talbot 12. Polarity in Plants Edited by K. Lindsey 13. Plastids Edited by S.G. Moller 14. Plant Pigments and their Manipulation Edited by K.M. Davies 15. Membrane Transport in Plants Edited by M.R. Blatt 16. Intercellular Communication in Plants Edited by A.J. Fleming 17. Plant Architecture and its Manipulation Edited by C. Turnbull 18. Plasmodesmata Edited by K.J. Oparka 19. Plant Epigenetics Edited by P. Meyer 20. Flowering and its Manipulation Edited by C. Ainsworth 21. Endogenous Plant Rhythms Edited by A. Hall and H. McWatters 22. Control of Primary Metabolism in Plants Edited by W.C. Plaxton and M.T. McManus 23. Biology of the Plant Cuticle Edited by M. Riederer Flowering and its Manipulation Edited by CHARLES AINSWORTH Department of Agricultural Sciences Imperial College Wye Campus Ashford Kent UK © 2006 by Blackwell Publishing Ltd Editorial Offices: Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK Tel: +44 (0)1865 776868 Blackwell Publishing Professional, 2121 State Avenue, Ames, Iowa 50014-8300, USA Tel: +1 515 292 0140 Blackwell Publishing Asia, 550 Swanston Street, Carlton, Victoria 3053, Australia Tel: +61 (0)3 8359 1011 The right of the Author to be identified as the Author of this Work has been asserted in accordance with the Copyright, Designs and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. First published 2006 by Blackwell Publishing Ltd ISBN-10: 1-4051-2808-9 ISBN-13: 978-14051-2808-7 Library of Congress Cataloging-in-Publication Data Flowering and its manipulation/edited by Charles Anisworth. p. cm. Includes bibliographical references. ISBN-13: 978-1-4051-2808-7 (hardback : alk. paper) ISBN-10: 1-4051-2808-9 (hardback : alk. paper) 1. Plants, Flowering of. I. Ainsworth, C. C. (Charles Colin), 1954- SB126.8.F58 2006 635.9 15233–dc22 2005022778 A catalogue record for this title is available from the British Library Set in 10/12 pt Times by Newgen Imaging Systems (P) Ltd. Chennai, India Printed and bound in India by Replika Press Pvt, Ltd, Kundli The publisher’s policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices. Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards. For further information on Blackwell Publishing, visit our website: www.blackwellpublishing.com Contents Contributors xiii Preface xv Part I. Core Development and Genetics 1 A developmental genetic model for the origin of the flower 3 DAVID A. BAUM and LENA C. HILEMAN 1.1 Introduction 3 1.2 What is a flower? 4 1.3 Phylogenetic and paleontological context 5 1.4 Evolutionary novelties of the flower 6 1.4.1 Bisexuality 6 1.4.2 Determinate/compressed axes 7 1.4.3 Perianth 7 1.5 Ordering the key steps in floral evolution 8 1.6 Developmental genetic background 9 1.6.1 Position and identity of the reproductive organs 9 1.6.2 Developmental regulation of the perianth 13 1.7 Models for the origin of bisexuality 14 1.8 Apical megasporophyll production on a microsporangiate axis? 16 1.9 The compression of the floral axis 18 1.10 The evolution of the perianth 19 1.11 The origin of a dimorphic perianth 20 1.12 Conclusion 21 References 22 2 Floral induction 28 REYNALD TREMBLAY and JOSEPH COLASANTI 2.1 Introduction 28 2.2 Floral transition is marked by developmental phase changes 28 2.3 Floral induction is mediated through multiple pathways 30 2.4 Photoperiodic floral induction provides a cue to seasonal changes 31 2.4.1 Photoreceptors transduce light signals 31 2.4.2 The circadian clock is self-reinforcing 32 2.4.3 Key genes integrate photoperiodic induction 32 vi CONTENTS 2.4.4 CO and FT gene function is conserved in other plant species 34 2.4.5 Photoperiod induction through CO-independent pathways 35 2.5 Autonomous pathway 36 2.5.1 FLOWERING LOCUS C integrates different floral inductive pathways 36 2.6 Vernalization 38 2.6.1 Mediation of vernalization in Arabidopsis by FLC repression 38 2.6.2 Vernalization in cereals 40 2.7 Hormones and other factors 41 2.7.1 Nutrient diversion theory of floral induction 41 2.7.2 Gibberellin 42 2.7.3 Long-distance floral inductive signals 44 2.7.4 Integration and commencement of the floral transition 45 2.7.4.1 LEAFY and APETALA1 45 2.7.4.2 TERMINAL FLOWER 1 45 2.7.4.3 Conservation of LFY function in higher plants 45 2.8 Perspective 46 References 46 3 Floral patterning and control of floral organ formation 49 ELENA M. KRAMER 3.1 Introduction 49 3.2 The ABC model of floral organ identity 49 3.2.1 The major genetic players in the ABC model 50 3.2.2 Members of the MADS-box transcription factor family 51 3.2.2.1 Redundant and complex functions among the floral MIKC MADS-box genes 53 3.2.3 Members of the AP2/EREBP transcription factor family 55 3.3 Regulating the expression of the floral organ identity genes 56 3.4 Conservation and modification of the ABC program 58 3.4.1 Floral organ identity gene function in Petunia 58 3.4.2 Floral organ identity gene function in Oryza 60 3.5 Sex determination as a modification of floral organ identity 62 3.6 Future perspectives 63 References 64 4 The genetic control of flower size and shape 71 LYNETTE FULTON, MARTINE BATOUX, RAM KISHOR YADAV and KAY SCHNEITZ 4.1 Introduction 71 4.2 Flower primordium outgrowth 73 CONTENTS vii 4.3 Regulating flower meristem size 74 4.3.1 Cell–cell communication, pattern formation in the meristem and meristem size 75 4.3.2 Cellular factors regulating floral meristem development 77 4.4 Early control of organogenesis in the flower 79 4.5 Generating organ boundaries 82 4.6 Floral organ size 84 4.7 Flower shape and symmetry 86 4.7.1 Floral determinacy 86 4.8 Dorsoventral symmetry 88 4.8.1 Petal asymmetry and contort aestivation 90 4.9 Outlook: to boldly go where no one has gone before ... 91 References 92 5 Inflorescence architecture – Moving beyond description to development, genes and evolution 98 SUSAN R. SINGER 5.1 Overview 98 5.2 Inflorescence typologies 98 5.3 Inflorescence development 104 5.3.1 Inflorescence meristem 104 5.3.2 Regulating determinacy 105 5.3.3 Regulating meristem identity 108 5.4 Evolution of inflorescence architecture 108 5.4.1 Teosinte 108 5.4.2 Cauliflower and Broccoli 109 5.4.3 Phenotypic plasticity 110 5.5 Future directions: modeling inflorescence architecture 111 References 111 Part II. Specialised Components of Development 6 Close, yet separate: patterns of male and female floral development in monoecious species 117 RAFAEL PERL-TREVES and PREM ANAND RAJAGOPALAN 6.1 Introduction 117 6.2 Ecological and evolutionary aspects of monoecious plant development 118 6.2.1 Evolution of diverse reproductive strategies in land plants 118 6.2.2 Selective forces that favor the evolution of unisexual flowers 119 6.2.3 Flexibility in sex ratios in monoecious plants 119 6.2.4 Relationship between monoecy and pollination 121 viii CONTENTS 6.2.5 The andromonoecious option: more compromises? 121 6.3 How do unisexual flowers develop? 122 6.3.1 Structural differences between male and female flowers 122 6.3.2 Unisexual flower development in maize 123 6.3.2.1 Development of the male and female florets 123 6.3.2.2 Mutations that affect stamen development: role of gibberellin 124 6.3.2.3 Mutations that affect pistil abortion 126 6.3.2.4 Cytokinin counteracts pistil abortion 127 6.3.2.5 Conservation of the maize sex determination pathway in other species 128 6.3.3 Unisexual flower development in cucumber 129 6.3.3.1 Cucumber