Developmental Biology NINTH EDITION SCOTT F. GILBERT
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Developmental Biology NINTH EDITION SCOTT F. GILBERT Swarthmore College and The University of Helsinki Sinauer Associates, Inc. a Publishers. Sunderland, Massachusetts USA
Developmental Biology NINT H EDITIO N SCOTT F. GILBERT Swarthmoro College and The University of Helsinki j ^ H Sinauer Associates, Inc. • Publishers • Sunderland, Massachusetts USA
Brief Contents PART I QUESTIONS Introducing Developmental Biology 1 CHAPTER 1 Developmental Anatomy 5 CHAPTER 2 Developmental Genetics 31 CHAPTER 3 Cell-Cell Communication in Development 69 PART II SPECIFICATION Introducing Cell Commitment and Early Embryonic Development 109 CHAPTER 4 Fertilization 121 CHAPTEr 5 Early Development in Selected Invertebrates 159 CHAPTER 6 The Genetics of Axis Specification in Drosophila 203 CHAPTER 7 Amphibians and Fish 247 ChaPTer8 Birds and Mammals 287 PART III THE STEM CELL CONCEPT Introducing Organogenesis 323 CHAPTER9 The Emergence of the Ectoderm 333 CHAPTER 10 Neural Crest Cells and Axonal Specificity 373 CHAPTER 11 Paraxial and Intermediate Mesoderm 413 CHAPTER 12 Lateral Plate Mesoderm and the Endoderm 445 CHAPTER 13 Development of the Tetrapod Limb 485 CHAPTER 14 Sex Determination 511 CHAPTER 15 Postembryonic Development 541 CHAPTER 16 The Saga of the germ Line 583 PART IV SYSTEMS BIOLOGY Expanding Developmental Biology to Medicine, Ecology, and Evolution 617 CHAPTER 17 Medical Aspects of Developmental Biology 625 CHAPTER 18 Developmental Plasticity and Symbiosis 659 CHAPTER 19 Developmental Mechanisms of Evolutionary Change 683
Brief Contents PART I QUESTIONS Introducing Developmental Biology 1 CHAPTER 1 Developmental Anatomy 5 CHAPTER 2 Developmental Genetics 31 CHAPTER 3 Cell-Cell Communication in Development 69 PART II SPECIFICATION Introducing Cell Commitment and Early Embryonic Development 109 CHAPTER 4 Fertilization 121 CHAPTER 5 Early Development in Selected Invertebrates 159 CHAPTER 6 The Genetics of Axis Specification in Drosophila 203 CHAPTER 7 Amphibians and Fish 241 CHAPTER 8 Birds and Mammals 287 PART III THE STEM CELL CONCEPT Introducing Organogenesis 323 CHAPTER 9 The Emergence of the Ectoderm 333 CHAPTER 10 Neural Crest Cells and Axonal Specificity 373 CHAPTER 11 Paraxial and Intermediate Mesoderm 413 CHAPTER 12 Lateral Plate Mesoderm and the Endoderm 445 CHAPTER 13 Development of the Tetrapod Limb 485 CHAPTER 14 Sex Determination^ 511 CHAPTER 15 Postembryonic Development 541 CHAPTER 16 The Saga of the Germ Line 583 PART IV SYSTEMS BIOLOGY Expanding Developmental Biology to Medicine, Ecology and Evolution 617 CHAPTER 17 Medical Aspects of Developmental Biology 625 CHAPTER 18 Developmental Plasticity and Symbiosis 659 CHAPTER 19 Developmental Mechanisms of Evolutionary Change 683
Contents PART QUESTIONS Introducing Developmental Biology 1 CHAPTER 7 CHAPTER 2 Developmental Anatomy 5 Developmental Genetics 31 The Cycle of Life 6 Evidence for Genomic Equivalence 32 A Frogs Life 6 H SIDELIGHTS SPECULATIONs The Basic Tools of Gametogenesis and fertilization 6 Developmental Genetics 32 Cleavage and gastrulation 7 Differential Gene Transcription 35 Organogenesis 10 Anatomy of the gene: Active and repressed Metamorphosis and gametogenesis 11 chromatin 36 " How Are You?" 12 Anatomy of the gene: Exons and introns 37 Comparative embryology 12 Anatomy of the gene: Promoters and enhancers 39 Epigenesis and preformation 12 Transcription factor function 42 the parts: The primary germ layers and I S/DELIGHTS SPECULATIONS Reprogramming Cells earlv organs 14 Changing Cell Differentiation through Embryonic The four principles of Karl Ernst von Baer 16 Transcription Factors 45 DNA Methylation and the Control of Keeping Track of Moving Cells: Fate Maps and Cell Lineages 17 Transcription 48 Fate maps 1g Mechanisms by which DNA methylation blocks transcription 49 Direct observation of living embryos 19 Inheritance and stabilization of DNa methvlation atterns 49 Genetic labeling 20 SIDELIGHTS SPECULATIONS Consequences of DNA Transgenic DNA chimeras 22 Methylation 50 Evolutionary Embryology 23 Differential RNA Processing 53 Embryonic homologies 24 Control of early development by nuclear RNA Medical Embryology and Teratology 27 selection 53 Genetic malformations and syndromes 27 Creating families of proteins through differential nRNA splicing 54 Disruptions and teratogens 28
Contents PART I QUESTIONS Introducing Developmental Biology 1 CHAPTER 1 Developmental Anatomy 5 The Cycle of Life 6 A Frog's Life 6 Gametogenesis and fertilization 6 Cleavage and gastrulation 7 Organogenesis 10 Metamorphosis and gametogenesis 11 "How Are You?" 12 Comparative embryology 12 Epigenesis and preformation 12 Naming the parts: The primary germ layers and early organs 14 The four principles of Karl Ernst von Baer 16 Keeping Track of Moving Cells: Fate Maps and Cell Lineages 17 Fate maps 19 Direct observation of living embryos 19 Dye marking 19 Genetic labeling 20 Transgenic DNA chimeras 22 Evolutionary Embryology 23 Embryonic homologies 24 Medical Embryology and Teratology 27 Genetic malformations and syndromes 27 Disruptions and teratogens 28 CHAPTER 2 Developmental Genetics 31 Evidence for Genomic Equivalence 32 • SIDELIGHTS & SPECULATIONS The Basic Tools of Developmental Genetics 32 Differential Gene Transcription 35 Anatomy of the gene: Active and repressed chromatin 36 Anatomy of the gene: Exons and introns 37 Anatomy of the gene: Promoters and enhancers 39 Transcription factor function 42 • SIDELIGHTS & SPECULATIONS Reprogramming Cells: Changing Cell Differentiation through Embryonic Transcription Factors 45 DNA Methylation and the Control of Transcription 48 Mechanisms by which DNA methylation blocks transcription 49 Inheritance and stabilization of DNA methylation patterns 49 • SIDELIGHTS & SPECULATIONS Consequences of DNA Methylation 50 Differential RNA Processing 53 Control of early development by nuclear RNA selection 53 Creating families of proteins through differential nRNA splicing 54
Splicing enhancers and recognition factors 56 Cell Signaling 79 Control of Gene Expression at the Level of Induction and competence 79 Translation 58 Cascades of induction: Reciprocal and sequential Differential mRNAlongevity 58 inductive events s0 elective inhibition of mRNa translation: Stored Instructive and permissive interactions 81 pithelial-mesenchymal interactions 82 microRNAs: Specific regulators of mRNA Paracrine Factors: The Inducer Molecules 84 translation and transcription 61 Signal transduction cascades: The response to m SIDELIGHTS SPECULatIoNs microRNAs in inducers 85 Transcriptional Gene Regulation 63 Fibroblast growth factors and the RTK pathway Control of rNA expression by cytoplasmic localization 64 The JAK-STAT pathway 88 Stored mRNAs in brain cells The Hedgehog family 90 Posttranslational regulation of gene expression 66 The Wnt family 92 The TGF-B superfamily 94 Other paracrine fa CHAPTER 3 I S/DELIGHTS SPECULATIONS Cell Death Pathways 96 Cell-Cell Communication in uxtacrine Signaling 98 Development 69 The Notch pathway: Juxtaposed ligands and receptors 98 Cell Adhesion 70 m SIDEU/GHTS SPECULATIONS Juxtacrine Signaling and Cell Patterning 99 Differential cell affinity 70 Maintaining the Differentiated State 101 The thermodynamic model of cell interactions 72 The Extracellular Matrix as a source of Cadherins and cell adhesion 73 Developmental Signals 102 L SIDELIGHTS SPECULATIONS Shape Change and Integrins: Receptors for extracellular matrix pithelial Morphogenesis: The Force Is Strong molecules 102 Epithelial-Mesenchymal Transition 105 Cell Migration 78 SPECIFICATION Introducing Cell Commitment PART and Early Embryonic Development 109 Levels of Commitment 109 Morphogen Gradients and Cell Specification 116 Autonomous Specification 110 Syncytial Specification 117 Conditional Specification 112 Summary 119 CHAPTER 4 External Fertilization in Sea Urchins 127 Fertilization: Beginning a New Sperm attraction: Action at a distance 128 The acrosome reaction 130 Organism 121 Recognition of the eggs extracellular coat 131 Fusion of the egg and sperm cell membranes 133 Structure of the Gametes 121 The fast block to polyspermy 135 Sperm 121 The slow block to polyspermy 136 The egg 125 Calcium as the initiator of the cortical granule Recognition of egg and sperm 127 acton
Splicing enhancers and recognition factors 56 Control of Gene Expression at the Level of Translation 58 Differential mRNA longevity 58 Selective inhibition of mRN A translation: Stored oocyte mRNAs 58 microRNAs: Specific regulators of mRNA translation and transcription 61 • SIDELIGHTS & SPECULATIONS microRNAs in Transcriptional Gene Regulation 63 Control of RNA expression by cytoplasmic localization 64 Stored mRNAs in brain cells 65 Posttranslational regulation of gene expression 66 CHAPTER 3 Cell-Cell Communication in Development 69 Cell Adhesion 70 Differential cell affinity 70 The thermodynamic model of cell interactions 72 Cadherins and cell adhesion 73 • SIDELIGHTS & SPECULATIONS Shape Change and Epithelial Morphogenesis: "The Force Is Strong in You" 76 Cell Migration 78 Cell Signaling 79 Induction and competence 79 Cascades of induction: Reciprocal and sequential inductive events 80 Instructive and permissive interactions 81 Epithelial-mesenchymal interactions 82 Paracrine Factors: The Inducer Molecules 84 Signal transduction cascades: The response to inducers 85 Fibroblast growth factors and the RTK pathway 85 The JAK-STAT pathway 88 The Hedgehog family 90 The Wnt familv 92 The TGF-fi superfamily 94 Other paracrine factors 95 • SIDELIGHTS & SPECULATIONS Cell Death Pathways 96 Juxtacrine Signaling 98 The Notch pathway: Juxtaposed ligands and receptors 98 • SIDELIGHTS & SPECULATIONS Juxtacrine Signaling and Cell Patterning 99 Maintaining the Differentiated State 101 The Extracellular Matrix as a Source of Developmental Signals 102 Integrins: Receptors for extracellular matrix molecules 102 Epithelial-Mesenchymal Transition 105 PART SPECIFICATION Introducing Cell Commitment and Early Embryonic Development 109 Levels of Commitment 109 Autonomous Specification 110 Conditional Specification 112 CHAPTER 4 : Beginning a New Organism 121 Structure of the Gametes 121 Sperm 121 The egg 125 Recognition of egg and sperm 127 Morphogen Gradients and Cell Specification 116 Syncytial Specification 117 Summary 119 External Fertilization in Sea Urchins 127 Sperm attraction: Action at a distance 128 The acrosome reaction 130 Recognition of the egg's extracellular coat 131 Fusion of the egg and sperm cell membranes 133 The fast block to polyspermy 135 The slow block to polyspermy 136 Calcium as the initiator of the cortical granule reaction 137