Summary of contents

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Summary of contents
Contents
Text acknowledgements
Figure acknowledgements
xi
xviii
xix
Chapter1
History and basic concepts
Chapter2
Development of the Drosophila body plan
31
Chapter3
Patterning the vertebrate body plan 1:
axes and germ layers
89
Chapter 4
Patterning the vertebrate body plan II:
the somites and early nervous System
149
Chapter 5
Development of nematodes, sea urchins,
ascidians, and slime molds
185
Chapter6
Plant development
225
Chapter7
Morphogenesis: change in form in
the early embryo
257
Chapter3
Cell differentiation and stem cells
297
Chapter9
Organogenesis
339
Chapter 10
Development of the nervous System
387
Chapter11
Germ cells, fertilization, and sex
421
Chapter12
Growth and post-embryonic development
451
Chapter13
Regeneration
475
Chapter14
Evolution and development
497
1
Kapitelzusammenfassungen
525
Glossar mit deutschen Erläuterungen
531
Index
545
Bibliografische Informationen
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Cimpter 1: History and basic concepts
Cimpter 2: Development of
the Drosophila body plan
The origins of developmental biology
1.1 Aristotle first defined the problem of epigenesis
and preformation
Drosophila life cycle and overall development
32
2.1 The early Drosophila embryo isa multinudeate
33
• Box 1A Basic stages of Xenopus loevis development
syncytium
1.2 Cell theory changed the conception of embryonic
development and heredity
2.2 Cellularization is followed by gastrulation,
segmentation, and the formation of the larval nervous
System
33
2.3 After hatching the Drosophila larva develops
through several larval stages, pupates. and then undergoes
morphogenesis to become an adult
34
2.4 Many developmental mutations have been
identified in Drosophila through induced mutation
and large-scale genetic screening
35
• Box 2A Mutagenesis and genetic screening strategy
for identifying developmental mutants in Drosophila
36
Setting up the body axes
37
37
1.3 Two main types of development were originally proposed
1.4 The discovery of induction showed that one group
of cells could determine the development of neighboring cells
i.s The studyof development was stimulated by
the Coming together of genetics and development
1.6 Development is studied mainly through a selection
of model organisms
9
1.7 The first developmental genes were identified as
spontaneous mutations
11
A conceptual tool kit
13
1.8 Development involves cell division. the emergence
of pattern, change in form, cell differentiation, and growth
13
2.s The body axes are set up while the Drosophila
embryo is still a syncytium
15
2.6 Maternal factors set up the body axes and direct
the early stage of Drosophila development
38
• Box 1B Germ layers
1.9 Cell behavior provides the link between gene
action and developmental processes
16
2.7 Three classes of maternal genes specify
the antero-posterior axis
40
1.10 Genes control cell behavior by specifying which
proteins are made
17
2.8 The bkoid gene provides an antero-posterior
gradient of morphogen
41
1.11 The expression of developmental genes is under
the control of cornplex control regions
18
2.9 The posterior pattem is controlled by the gradients
of Nanos and Caudal proteins
42
1.12 Development is progressive and the fate of cells
becomes determined at different times
19
43
1.« Inductive interactions can make cells different
from each other
22
2.10 The anterior and posterior extremities of
the embryo are specified by cell-surface receptor
activation
23
2.11 The dorso-ventral polarity of the embryo is
specified by localization of maternal proteins in
the egg vitelline envelope
44
1.14 The response to inductive Signals depends on
the State of the cell
i.is Patterning can involve the interpretation
of positional information
23
2.12 Positional information along the dorso-ventral
axis is provided by the Dorsal protein
45
1.16 Lateral inhibition can generate spacing patterns
25
• Box 2B TheToil signaling pathway. a multifunctional
pathway
46
1.17 Localizationofcytoplasmicdeterminantsand
asymmetric cell division can make cells different
from each other
25
Localization of maternal determinants during
47
i.is The embryo contains a generative ratherthan
a descriptive program
26
1.19 The reliability of development is achieved
by a variety of means
27
1.20 The complexity of embryonic development
is due to the complexity of cells themselves
27
oogenesis
2.13 The antero-posterior axis of the Drosophila egg
is specified by Signals from the preceding egg chamber
and by interactions of the oocyte with follicle cells
48
2.14 The dorso-ventral axis of the egg is specified by
movement of the oocyte nucleus followed by signaling
between oocyte and follicle cells
51
XII
CONTENTS
Patterning the early embryo
52
• Box 3A Polar bodies
93
2.15 The expression of zygotic genes along
the dorso-ventral axis is controlled by Dorsal protein
52
3.2 The zebrafish embryo develops around a large,
undivided yolk
96
2.16 The Decapentaplegic protein acts as a morphogen
to pattern the dorsal region
55
3.3 The early chicken embryo develops as a flat disc
of cells overlying a massive yolk
98
2.17 The antero-posterior axis is divided up into broad
regions by gap-gene expression
57
• Box 3B Large-scale mutagenesis in zebrafish
99
104
2.18 Bicoid protein provides a positional Signal for
the anterior expression of hunchback
57
3.4 Early development in the mouse involves
the allocation of cells to form the placenta and
extra-embryonic membranes
2.19 The gradient in Hunchback protein activates
and represses other gap genes
58
Setting up the body axes
108
• Box 2C P-element-mediated transformation
59
3.5 The animal-vegetal axis ismaternally
determined in Xenopus and zebrafish
109
Activation of the pair-rule genes and
the establishment of parasegments
61
110
2.20 Parasegments are delimited by expression of
pair-rule genes in a periodic pattern
61
3.6 Localizedstabilizationofthetranscriptional
regulator ß-catenin specifies the future dorsal side
and the location of the main embryonic Organizer
in Xenopus and zebrafish
2.21 Gap-gene activity positions stripes of pair-rule
gene expression
62
• Box3C Intercellular Signals in development
111
• Box3D In situ detection of gene expression
112
Segmentation genes and compartments
65
3.7 Signaling centers develop on the dorsal side
of Xenopus and zebrafish
115
2.22 Expression of the engrailed gene delimits
a cell-lineage boundary and defines a compartment
65
3.8 The antero-posterior and dorso-ventral axes
of the chick blastoderm are related to the primitive streak
117
3.9 The axes of the mouse embryo are not recognizable
early in development
119
3.10 The bilateral symmetry of the early embryo is broken
to produce left-right asymmetry of internal organs
121
The origin and specification of the germ layers
125
3.11 Afatemapof the amphibian blastula is
constructed by following the fate of labeled cells
125
3.12 The fate mapsofvertebrates are variations
on a basic plan
127
3.13 Cells of early vertebrate embryos do not yet
have their fates determined and regulation is possible
128
• Box 3E Producing developmental mutations in mice
130
• Box 2D Genetic mosaics and mitotic recombination
68
2.23 Segmentation genes stabilize parasegment
boundaries and set up a focus of signaling at
the boundary that pattems the segment
70
2.24 Insect epidermal cells become individually polarized
in an antero-posterior direction in the plane of the epithelium
73
• Box2E Planarcellpolarity
75
2.25 Some insects use different mechanisms for
patterning the body plan
76
Specification of segment identity
78
2.26 Segment identity in Drosophila is specified by
genes of the Antennapedia and bithorax complexes
78
2.27 Homeotic selector genes of the bithorax complex
are responsible for diversification of the posterior
Segments
79
3.14 In Xenopus the endoderm and ectoderm are
specified by maternal factors, but the mesoderm is
induced from ectoderm by Signals from the vegetal region
2.28 The Antennapedia complex controls specification
of anterior regions
80
3.15 Mesoderm induction occurs during a limited
period in the blastula stage
132
2.29 The order of Hox gene expression corresponds to
the order of genes along the chromosome
81
3.16 Zygotic gene expression is turned on at
the mid-blastula transition
133
3.17 Mesoderm-inducing and patterning Signals are
produced by the vegetal region, the Organizer,
and the ventral mesoderm
134
3.18 MembersoftheTGF-ßfamily have been identified
as mesoderm inducers
136
3.19 The dorso-ventral patterning of the mesoderm
involves the antagonistic actions of dorsalizing and
ventralizing factors
137
3.20 Mesoderm induction and patterning in the chick
and mouse occurs during primitive-streak formation
139
3.21 Gradients in signaling proteins and threshold
responses could pattern the mesoderm
140
2.30 The Drosophila head region is specified by genes
other than the Hox genes
81
• Box 2F Targeted gene expression and misexpression
screening
82
Chapter 3: Patterning the vertebrate
body plan I: axes andgerm layers
Vertebrate life cydes and outlines of development
90
3.1 The frog Xenopus/aev/sis the modelamphibian
for developmental studies
92
130
CONTENTS
Chapter 4: Patterning the vertebrate
body plan II: the somites and early
nervous System
xiii
5.6 Vulval development is initiated by the induction
of a small number of cells by short-range Signals
from a Single inducing cell
199
Echinoderms
202
Somite f o r m a t i o n and antero-posterior patterning
151
151
5.7 The sea urchin embryo develops into
a free-swimming larva
202
4.1 Somites are formed in a well defined order along
the antero-posterior axis
155
5.8 The sea urchin egg is polarized along
the animal-vegetal axis
203
4.2 Identity of somites along the antero-posterior axis
is specified by Hox gene expression
156
5.9 The oral-aboral axis in sea urchins is related
to the plane of the first cleavage
205
• Box 4A The Hox genes
• Box4B Gene targeting: insertional mutagenesis
and gene knock-out
158
5.10 The sea urchin fate map is finely specified,
yetconsiderable regulation is possible
206
4.3 Deletion or overexpression of Hox genes causes
changes in axial patterning
162
5.11 The vegetal region ofthe sea urchin embryo
acts as an Organizer
207
4.4 Hox gene activation is related to a timing
mechanism
163
5.12 The sea urchin vegetal region is specified
by nuclear accumulation of ß-catenin
208
4.5 The fate ofsomite cells is determined by Signals
from the adjacent tissues
164
5.13 The genetic control of endomesoderm
specification is known in considerable detail
210
The role of the Organizer and neural induction
166
Ascidians
212
4.6 The inductive capacity of the Organizer changes
during gastrulation
167
5.14 In ascidians, muscle is specified by localized
cytoplasmic factors
214
4.7 The neural plate is induced in the ectoderm
169
215
4.8 The nervous System can be patterned by Signals
from the mesoderm
173
5.15 Mesenchyme and notochord development in
ascidians require Signals from the endoderm
Cellular slime molds
217
4.9 There is an Organizer at the midbrain-hindbrain
boundary
175
s.16 Patterning ofthe slime moldslug involves cell
sorting and positional signaling
218
4.10 The hindbrain is segmented into rhombomeres
by boundaries of cell-lineage restriction
175
5.17 Chemical Signals direct cell differentiation
in the slime mold
219
4.11 Neural crest cells arise from the borders
ofthe neural plate
177
4.12 Hox genes provide positional information
in the developing hindbrain
178
4.13 The embryo is patterned by the neurula stage
into organ-forming regions that can still regulate
179
Chapter 6: Plant development
6.1 The modelplant/4rafa/c/ops/stho//onohasa short
life cycle and a small diploid genome
226
Embryonic development
228
Chapter 5: Development of nematodes,
sea urchins, ascidians, and slime molds
6.2 Plant embryos develop through several
distinct stages
228
• Box6A Angiosperm embryogenesis
229
Nematodes
186
231
• Box5A Gene silencing by RNA interference
189
6.3 Gradients ofthe Signal molecule auxin establish
the embryonic apical-basal axis
6.4 Plant somatic cells can give rise to embryos
and seedlings
232
B Box 6B Transgenic plants
234
5.1 The antero-posterior axis in C. elegans is
determined by asymmetric cell division
190
5.2 The dorso-ventral axis in C. elegans is
determined by cell-cell interactions
191
Meristems
234
53 Both asymmetric divisions and cell-cell interactions
specify cell fate in the early nematode embryo
193
6.5 A meristem contains a small central Zone
of self-renewing stem cells
235
5.4 A small düster of Hox genes specifies cell fate
along the antero-posterior axis
195
6.6 The size of the stem-ceii area in the meristem is kept
constant by a feedback loop to the organizing center
235
5.5 The timing ofevents in nematode development
is under genetic control that involves microRNAs
196
6.7 The fate of cells from different meristem layers
can be changed by changing their position
237
• Box SB Gene silencing by microRNAs
197
6.8 A fate map for the embryonic shoot meristem
can be deduced using clonal analysis
238
CONTENTS
6.9 Meristem development is dependent on Signals
from other parts ofthe plant
240
7.11 Vertebrate gastrulation involves several different
types of tissue movement
276
6.10 Gene activity patterns the proximo-distal and
adaxial-abaxial axes of leaves developing from the
shoot meristem
240
7.12 Convergent extension and epiboly are
due to different types of cell intercalation
280
6.11 The regulär arrangementof leaves ona stem
and trichomes on leaves is generated by competition
and lateral inhibition
242
Neural-tube formation
283
7.13 Neural-tube formation is driven by changes
in cell shape and cell migration
284
6.12 Root tissues are produced from Arabidopsis
root apical meristems by a highly stereotyped pattern
of cell divisions
243
Flower development and control of flowering
246
6.13 Homeotic genes control organ identity
in the flower
246
• Box 6C The basic model for the patterning of
the Arabidopsis flower
249
6.14 The Antirrhinum flower is patterned dorso-ventrally
as well as radially
250
6.15 The internal meristem layer can specify floral
meristem patterning
251
6.16 The transition of a shoot meristem to a floral
meristem is under environmental and genetic control
251
Cell migration
286
7.14 Neural crest migration is controlled by
environmental cues and adhesive differences
286
7.15 Slime mold aggregation involves chemotaxis
and Signal propagation
288
Directed dilation
290
7.16 Later extension and stiffening of the notochord
occurs by directed dilation
290
7.17 Circumferential contraction of hypodermal cells
elongates the nematode embryo
291
7.18 The directionof cell enlargement can determine
the form of a plant leaf
292
Chapter 3: Cell differentiation
and stem cells
Chapter 7: Morphogenesis: change
in form in the early embryo
Cell adhesion
258
• Box7A Cell-adhesion molecules and cell junctions
259
7.1 Sorting out of dissociated cells demonstrates
differences in cell adhesiveness in different tissues
260
7.2 Cadherins can provide adhesive specificity
261
Cleavage and formation ofthe blastula
262
7.3 The asters ofthe mitotic apparatus determine
the plane of cleavage at cell division
263
7.4 Cells become polarized in early mouse and
sea urchin blastulas
264
7.5 Ion transport is involved in fluid accumulation
in the frag blastocoel
• Box 8A DNA microarrays for studying gene expression
299
The control of gene expression
301
8.1 Control oftranscription involves bothgeneral
and tissue-specific transcriptional regulators
301
8.2 External Signals can activate genes
303
8.3 Maintenance and inheritance of patterns of gene
activity may depend on chemical and structural
modifications to chromatin as well as on regulatory
proteins
305
Models of cell differentiation
309
8.4 All blood cells are derived from multipotent
stem cells
310
266
267
8.5 Colony-stimulating factors and intrinsic changes
control differentiation of the hematopoietic lineages
312
7.6 Internal cavities can be created by cell death
269
7.7 Gastrulation in the sea urchin involves cell
migration and invagination
269
8.6 Developmentally regulated globin gene expression
is controlled by regulatory sequences far distant from
the coding regions
314
Castrulation movements
270
8.7 Differentiation of cells that make antibodies involves
irreversible DNA rearrangement
316
• Box 7B Change in cell shape and cell movement
7.8 Mesoderm invagination in Drosophila is due to
changes in cell shape that are controlled by genes
that pattern the dorso-ventral axis
273
8.8 The epithelia of adult mammalian skin and gut
are continually replaced by derivatives of stem cells
318
275
8.9 Afamilyof genes can activate muscle-specific
transcription
319
7.9 Germ-band extension in Drosophila involves
myosin-dependent intercalation
276
8.10 The differentiation of muscle cells involves
withdrawal from the cell cycle, but is reversible
320
7.10 Dorsal closure in Drosophila and ventral closure
in C elegans are brought about by the action of
filopodia
8.11 Skeletal muscle and neural cells can be renewed
from stem cells in adults
321
CONTENTS
XV
8.12 Embryonic neural crest cells differentiate into
a great variety of different cell types
322
9.16 Drosophila wing epidermal cells show planar
cell polarity
363
8.13 Programmed cell death is under genetic control
324
9.17 The leg disc is patterned in a similar manner
to the wing disc, except for the proximo-distal axis
363
The plasticity of gene expression
327
327
9.18 Butterfly wing markings are organizedby
additional positional fields
364
8.14 Nuclei of differentiated cells can support
development
329
9.19 The segmental identity of imaginal discsis
determined by the homeotic selector genes
366
8.15 Patterns ofgene activity in differentiated cells
can be changed by cell fusion
330
9.20 Patterning of the Drosophila eye involves
cell—cell interactions
367
8.16 The differentiated state of a cell can change by
transdifferentiation
8.17 Embryonic stem cells can proliferate and
differentiate into many cell types in culture
332
9.21 Activation ofthe gene eyeless can initiate
eye development
8.18 Stem cells could be a key to regenerative
medicine
332
Chapter 9: Organogenesis
Internal Organs: blood vessels, lungs, kidneys,
369
371
heart, and teeth
9.22 The vascular system develops by vasculogenesis
followed by angiogenesis
372
9.23 The tracheae of Drosophila and the lungs of
vertebrates branch using similar mechanisms
374
9.24 The development of kidneytubules involves
reciprocal induction by the ureteric bud and surrounding
mesenchyme
375
The vertebrate l i m b
340
9.1 The vertebrate limb develops from a limb bud
340
9.2 Patterning of the limb involves positional information
341
9.3 Genes expressed in the lateral plate mesoderm
are involved in specifying the position and type
of limb
341
9.25 The development ofthe vertebrate heart
involves specification of a mesodermal tube that is
patterned along its long axis
377
9.4 The apical ectodermal ridge is required for limb
outgrowth
343
9.26 A homeobox gene code specifies tooth identity
379
9.5 The polarizing region specifies position along
the limb's antero-posterior axis
345
• Box 9A Positional information and morphogen
gradients
347
Chapter 10: Development of
the nervous system
9.6 Position along the proximo-distal axis may be
specified by a timing mechanism
349
9.7 The dorso-ventral axis is controlled by the ectoderm
350
9.8 Different interpretations of the same positional
Signals give different limbs
Specification of cell identity in the nervous system
388
10.1 Neurons in Drosophila arise from proneural clusters
388
390
351
10.2 Asymmetric cell divisions and timed changes
in gene expression are involved in the development
ofthe Drosophila nervous system
351
10.3 The neuroblasts of the sensory organs of adult
Drosophila are already specified in the imaginal dises
392
9.9 Homeobox genes also provide positional values
for limb patterning
353
10.4 The vertebrate nervous system is derived from
the neural plate
392
9.10 Self-organization may be involved in
the development of the limb bud
354
IO.S Specification of vertebrate neuronal precursors
involves lateral inhibition
393
9.11 Limb muscle is patterned by the connective
tissue
355
10.6 Neurons are formed in the proliferative zone
of the neural tube and migrate ourwards
394
• Box 9B Reaction-diffusion mechanisms
9.12 The initial development of cartilage, muscles.
and tendons is autonomous
356
396
9.13 Joint formation involves secreted Signals
and mechanical Stimuli
357
10.7 The pattern of differentiation of cells along
the dorso-ventral axis of the spinal cord depends
on ventral and dorsal Signals
9.14 Separation of the digitsis the result
of programmed cell death
357
Insect w i n g s , legs. and eyes
358
9.15 Positional Signals from the antero-posterior
and dorso-ventra! compartment boundaries pattern
the wing imaginal disc
359
Neuronal migration
401
10.8 The growth cone controls the path taken
by the growing axon
402
10.9 Motor neurons from the spinal cord make
muscle-specific connections
403
10.10 Axons crossing the midline are both
attracted and repelled
405
CONTENTS
10.11 Neurons from the retina make ordered
connections on the tectum to form a retino-tectal map
406
Synapse formation and refinement
409
10.12 Synapse formation involves reciprocal
interactions
411
10.13 Many motor neurons die during normal development
412
10.14 Neuronal cell death and survival involve both
intrinsic and extrinsic factors
10.15 The map from eye to brain is refined by neural
activity
Chapter 12: Growth and post-embryonic
development
Growth
451
12.1 Tissues can grow by cell proliferation,
cell enlargement, or accretion
452
413
12.2 Cell proliferation can be controlled by
an intrinsic program
452
414
12.3 Organ size can be controlled by external
Signals and intrinsic growth programs
454
12.4 Organ size may be determined by absolute
dimension rather tfian cell number
455
12.5 Growth can be dependent on growth hormones
457
12.6 Growth ofthe long bones occurs in the growth
plates
458
Chapter 11: Germ cells, fertilization,
and sex
The development of germ cells
422
11.1 Germ-cell fate can be specified byadistinct
germplasm in the egg
422
12.7 Growth of vertebrate striated muscle is dependent
ontension
460
11.2 Pole plasm becomes localized at the posterior
end ofthe Drosophila egg
425
12.8 Cancer can result from mutations in genes
that control cell multiplication and differentiation
461
11.3 Germ cells migrate from their site oforigin
to the gonad
425
12.9 Hormones control many featuresof plant growth
463
Molting and metamorphosis
465
11.4 Germ-cell differentiation involves a reduction
in chromosome number
426
12.10 Arthropods have tomolt in order to grow
465
11.5 Oocyte development can involve gene
amplification and contributions from other cells
427
12.11 Metamorphosis is under environmental
and hormonal control
466
11.6 Some genes Controlling embryonic
growth are imprinted
427
Aging and senescence
469
12.12 Genes can alter the timing of senescence
470
Fertilization
432
471
11.7 Fertilization involves cell-surface interactions
between egg and sperm
432
12.13 Cultured mammalian cells undergo cell
senescence
11.8 Changes in the egg membrane at fertilization
block polyspermy
434
11.9 A calcium wave initiated at fertilization results
in egg activation
435
Determination ofthe sexual phenotype
437
11.10 The primary sex-determining gene in mammals
is on the Y chromosome
Chapter 13: Regeneration
Limb and organ regeneration
476
13.1 Vertebrate limb regeneration involves cell
dedifferentiation and growth
477
13.2 The limb blastema gives rise to structures with
positional values distal to the Site of amputation
480
437
438
13.3 Retinoic acid can change proximo-distal
positional values in regenerating limbs
482
11.11 Mammalian sexual phenotype is regulated
by gonadal hormones
439
13.4 Insect limbs intercalate positional values
by both proximo-distal and circumferential growth
483
11.12 The primary sex-determining Signal in Drosophila
is the number of X chromosomes, and is cell autonomous
441
13.5 Heart regeneration in the zebrafish does not
involve dedifferentiation
486
11.13 Somatic sexual development in Caenorhabditis
is determined by the number of X chromosomes
442
13.6 The mammalian peripheral nervous system
can regenerate
486
11.14 Most flowering plants are hermaphrodites,
but some produce unisexual flowers
i i . i s Germ-cell sex determination can depend both
on cell Signals and genetic constitution
443
Regeneration in Hydra
488
488
11.16 Variousstrategiesareusedfordosage
compensation of X-Iinked genes
444
13.7 Hydra grows continuously but regeneration
does not require growth
13.8 The head region of Hydra acts both as an
organizing region and as an inhibitorof inappropriate
head formation
489
CONTENTS
XVII
13.9 Head regeneration in Hydra can be accounted
for in terms of two gradients
490
14.6 Changes in Hox genes have generated the
elaboration of vertebrate and arthropod body plans
510
13.10 Genes Controlling regeneration in Hydra are
similar to those expressed in animal embryos
492
14.7 The position and number of paired appendages in
insects is dependent on Hox gene expression
513
14.8 The basic body plan ofarthropods and vertebrates
is similar, but the dorso-ventral axis is inverted
514
14.9 Evolution ofspatial pattern may bebasedon just
a few genes
516
Changes in the t i m i n g of developmental processes
517
14.10 Changes in growth can alter the shapes
oforganisms
517
14.11 The timing of developmental events has
changed during evolution
517
The evolution of development
520
14.12 Howmulticellularorganisms evolved from
single-celled ancestors is still highly speculative
520
ChnptGr 14: Evolution and development
14.1 The evolution of life histories has implications
for development
500
The evolutionary modification of embryonic
501
development
14.2 Embryonic structures have acquired new functions
during evolution
502
14.3 Limbs evolved from fins
504
14.4 Vertebrate and insect wings make use of
evolutionarily conserved developmental mechanisms
508
14.5 Hox gene complexes have evolved through gene
duplication
508
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