OXFORD Principles of Development Fourth edition Lewis Wolpert Cheryl! Tickle ies Peter Lawrence Elliot Meyerowitz pa Elizabeth Robertson Jim Smith Thomas JessellPrinciples of Development Fourth Edition Lewis Wolpert | Cheryll Tickle Thomas Jessell Peter Lawrence Elliot Meyerowitz Elizabeth Robertson Jim Smith OXFORD UNIVERSITY PRESSOXFORD UNIVERSITY PRESS (Great Clarendon Street, Oxford 0x2 60? Oxford University Press isa department of the University of Oxford Ie furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York ‘utekland Cape ‘Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipel Toranta With otfices in ‘Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary aly Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press inthe UK and in certain other eounteies Published in the United States by Oxford University Press Ine., New York (© Oxford University Press 2001 “The moral rights ofthe authors have been asserted Database right Oxford University Press (maker) 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, Without the prior permission in writing of Oxford University Peess, ‘ras expressly permitted by law, or under terms agreed withthe appropriate reprographies rights organization. Enquiries concerning reproduction ‘outside the seape af the above should he sent tothe Rights Department, Oxford University Pres, at the address above You must not circulate this book in any other binding or cover and you must impose the sume condition on any aca Bais Library Cataloguing in Publication Data Data ava able Library of Congress Cataloging in Publication Data Data available Typeset by Techset Composition Lid Printed in the United states om acid-fee paper by Courier, Kendallville, IN ISBN 978-1 ISBN 978-1 19-954907-8 (pbk) 19-955428-7 (Mb) las79me64a2About the authors Lewis Wolpert is Emeritus Professor of Biology as Applied to Medicine, in the Depart- ‘ment of Anatomy and Developmental Biology, University College London, London, UK. He is the author of The Triumph of the Embryo, A Passion for Science, The Unnatural Nature of Science, and Six Impossible Things Before Breakjest. Cheryll Tickle is Foulertan Research Professor of The Royal Society at the University of Bath, Bath, UK, Thomas Jessell is Professor of Biochemistry and Molecular Biophysics, a member of the Center for Neurobiology and Behaviour, and a Howard Hughes Medical Institute investigator at the Department of Biochemistry and Molecular Biophysics, University of Columbia Medical Center, New York, USA. He is an author of Principles of Neural Science and Essentials of Neural Science and Behaviour. Peter Lawrence is in the Department of Zoology, University of Cambridge and Emeritus member of the Medical Research Council Laboratory of Molecular Biology, Cambridge, UK. He is the author of The Making of a Fly Elliot Meyerowitz is the George W. Beadle Professor of Biology and Chair of the Divi. sion of Biology at the California Institute of Technology, Pasadena, CA, USA. Elizabeth Robertson is a Wellcome Trust Principal Fellow and Professor at the Sir William Dunn School of Pathology at the University of Oxford, Oxford, UK, ‘im Smith is Director of the Medical Research Council National Institute for Medical Research, London, UK. Eleanor Lawrence is a freelance science writer and editor, Matthew MeClements is an illustrator who specializes in design for scientific, techni eal, and medical communication,This page intentionally left blankSummary of contents Preface v About the authors vi Contents xi Reviewer acknowledgements xix Figure acknowledgements xx Chapter 1. History and basic concepts 1 Chapter 2 Development of the Drosophila body plan 35. Chapter 3. Vertebrate development k life cycles and experimental ‘techniques 93 Chapter 4. Vertebrate development I: axes and germ layers 128 Chapter 5 Vertebrate development Il patterning the early nervous system and the somites 173 Chapter 6 Development of nematodes, sea urchins, and ascidians ais Chapter 7. Plant development 255 Chapter 8 Morphogenesis: change in form in the early embryo 269 Chapter 9 Germ cells, fertilization, and sex 329 Chapter 10. Cell differentiation and stem cells 365, Chapter 11 Organagenesis, au Chapter 12. Development of the nervous system 468 Chapter 13. Growth and post-embryonic development 505, Chapter 14. Regeneration 535 Chapter 15. Evolution and development 556 Glossary 589 Index 605This page intentionally left blankContents Preface About the authors ‘Summary of contents Reviewer acknowledgements Figure acknowledgements Chapter 1 History and basic concepts Box 1A Basic stages of Xenopus laevis development The origins of developmental biology 1.1 Aristotle fist defined the problem of epigenesis and reformation 1.2 Coll theory changed the conception of embryonic development and heredity 1.3 Two main types of development were originally proposed 1 Box 18 The mitotic cell cycle 1.4 The discovery of induction showed that one group of cells could determine the development of neighboring cells 1S The study of development was stimulated by the coming together of genetics and development 1L6 Development is studied mainly through selected madet organisms 1.7 The first developmental genes were identified as spontaneous mutations Summary A conceptual tool kit 1.8 Development involves the emergence of pattern, change in form, cell differentiation, and growth Box 1C Germ layers 1,8 Cell behavior provides the link between gene action and developmental processes 41.10 Genes control cell behavior by specifying which proteins are made 1.11 The expression of developmental genes is under tight, control Box 1D Tracking gene expression in embryos 1.12 Development is progressive and the fate of cells, becomes determined at diferent times 11:3 Inductive interactions can make ces different from each other 1.14 The response to inductive signals depends on the state of the cell v vil ix xix xx i u 3B B 4 15 v7 v7 19 20 a 23 2s 1.15 Patterning can involve the interpretation of positional information 1 Box 2E Signal transduction and intracellular signaling 1.16 Lateral inhibition can generate spacing patterns 1.17 Localization of cytoplasmic determinants and asymmetric cell vision can make daughter cells dierent from each other 1m Box 2F When development goes awry 21.18 The embryo contains a generative rather than & descriptive program 1.19 The reliability of development is achieved by a variety of means 1.20 The complexity of embryonic development is due ‘to the complexity of cells themselves £1.21 Development is intimately involved in evolution ‘summary ‘Summary to Chapter 1 Chapter 2. Development of the Drosophila body plan Drosophilalite cycle and overall development 2:1 The early Drosophila embryo is a multinucleate syncytium 2.2 Cellularization is followed by gastrulation and segmentation 2.3 After hatching, the Drosophila larva develops through ‘several arval stages, pupates, and then undergoes ‘metamorphosis to become an adult 2.4 Many developmental genes have been identified in Drosophila through induced large-scale genetic screening Setting up the body axes 2.5 The body axes are set up while the Drosophito embryo is stil a syncytium 2.6 Maternal factors set up the body axes and direct the ‘early stage of Drosophila development 1H Box 2A Mutagenesis and genetic screening strategy ‘or identitying developmental mutants in Drosophila 2.7 Thee classes of maternal genes specify the antero- posterior axis 2.8 Bicold protein provides an antero-posterior gradient of a smoiphogen 25 26 27 2 28 29 30 30 31 32 2 35 36 6 38 38 39 40 40 4a 42 B 4Contents 2.9 The posterior pattems controlled by the gradients of Nanos and Caudal proteins 2.20 The antetior and posterior extremities of the embryo are specified by cell-surface receptor activation 2.11 The dorso-ventral polarity of the embryo is specified by localization of maternal proteins inthe egg vitelline envelope 2.12 Positional information along the dorso-ventral axis. is provided by the Dorsal protein 1 Box 28 The Toll signaling pathway: a multifunctional pathway Summary Localization of maternal determinants during oogenesis 2.13 The antero-posterior axis of the Drosophila egg is specified by signals from the preceding egg chamber and. by interactions ofthe oocyte with follicle cells 2.14 Localization of maternal mRNAS to either end of the egg depends on the reorganization ofthe oocyte cytoskeleton 2.15 The corso-ventral axis of the egg is specified by ‘movement of the oocyte nucleus followed by signaling between oocyte and follicle cells Summary Patterning the early embryo 2.16 The antero-posterior axis is divided up into broad regions by gap-gene expression 2.17 Bicoid protein provides a positional signal for the anterior expression of zygotic hunchback 2.18 The gradient in Hunchback protein activates and represses other gap genes 2.19 The expression of zygotic genes along the dorso ventral axis is contollee by Dersal pratela 1H Box 2¢ P-element-mediated transformation 1m Box 2D Targeted gene expression and misexpression screening 2.20 The Decapentaplegic protein acts as a morphogen tapattern the dorsal region Summary Activation of the pair-rule genes and the establishment of parasegments 2.21 Parasegments ae delimited by expression of pai-rule jgenes in aperiodic pattern 2.22 Gap-gene activity positions stripes of pair-rule gene expression Summary Segmentation genes and compartments 2.23 Expression of the engrailed gene delimits a celhlineage boundary and defines a compartment 1m Box 2E Genetic mosaics and mitotic recombination 46 4 48 49 50 50 SL 52 53 54 56 58 57 57 59 60 el 6 6 66 66 ee 70 70 70 a 2.24 Segmentation genes stabilize parasegment boundaries ‘and set up a focus of signaling at the boundary that pattems the segment 2.25 Insect epidermal ces become individually polarized in an antero-posterior direction in the plane of the epithelium 1m Box 2 Planar cel polarity in Drosophila 2.26 Some insects use different mechanisms fer patterning ‘the body plan ‘summary ‘Specification of segment identity 2.27 Segment identity in Drosophilais specified by Hox genes 2.28 Homeotic selector genes of the bithorax complex are responsible for diversification of the posterior segments 2.29 The Antennapedia complex controls specification of. anterior regions 2.30 The order of Hox gene expression corresponds to the ‘order of genes along the chromosome 2.31 The Drosophila head region is specified by genes other than the Hox genes ‘summary ‘Summary to Chapter 2 Chapter 3. Vertebrate development and experimental techniques Vertebrate life cycles and outlines of development life cycles 3.1 The frog Xenopus laevisis the model amphibian for developmental studies 3.2 The zebrafish embryo develops around a large mass of yolk 3.3 Birds and mammals resemble each other and citfer trom Xenopusin some important features of early development 3.4 The early chicken embryo develops as a fat disc of cells overiying a massive yolk 3.5 Early development in the mouse involves the allocation ‘of cells to form the placenta and extra-embryonic membranes Experimental approaches to stud development i vertebrate 3.6 Not all techniques are equally applicable to all vertebrates 1 Box 3A Gene-expression profiling by DNA microarray 3.7 Fate mapping and lineage tracing reveal which cells in ‘the early embryo give rise to which adult structures 18 Box 38 Insertional mutagenesis and gene knock-outs in mice: the Cre/loxP system 3.8 Developmental genes can be identified by spontaneous ‘mutation and by large-scale mutagenesis screens. 1m Gox 3C Large-scale mutagenesis in zebrafish 4 7 78 79 20 al aL 82 a4 24 85 85 86 94 96 101 103 103 109 3 ua us uy us ug 120Contents, 3.9 Transgenic techniques enable animals to be produced with mutations in specific genes 3.10 Gene function can also be tested by transient transeenesis and gene silencing 3.11 Gene regulatory networks in embryonic development can be revealed by chromatin immunopreciptation techniques Summary to Chapter 3 Chapter 4 Vertebrate development Il: axes and germ layers Setting up the body axes 4.1 The animal-vegetal axis is maternally determined in Xenopus and zebrafish 4.2 Localized stabilization of the transcriptional regulator B-catenin specifies the futute dorsal side and the location of the main embryonic organizer in Xenopus and zebrafish 1m Box 4A Intercellular protein signals in vertebrate development 4.3 Signaling centers develop on the dorsal side of Xenopus and zebrafish blastulas 4.4 The antero-posterior and dorso-ventral axes of the chick blastoderm are related tothe primitive streak 4.5 The definitive antero-posterior and dorso-ventral axes. of the mouse embryo are not recognizable early in development 4.6 Movement of the distal visceral endaderm indicates the rota gee ration in @<] d-a-m @ ae oemels Fig. 41.4 Some preformationists believed that an homunculus was curled up in the head of each sperm, {an imaginative drawing, ofter Nicholas Harspeler (1694). Fig. 4.5 The distinction between germ cells and somatic cells. In each generation germ cells give rise to both somatic cells and germ cals, but inheritance Is through the germ cells only (first pane), Changes that ‘accur due toa mutation (26) ina somatic coll can be passed on to its daughter cells but do not affect the germline, as shown in the second panel. In contrast, a mutation in the germline (green will be present in every Cell in the body ofthe new organism to wich that cll contributes, and will also be passed on to future generations through the jermline, as shown inthe third panel