Welcome to Scribd, the world's digital library. Read, publish, and share books and documents. See more ➡
Download
Standard view
Full view
of .
Add note
Save to My Library
Sync to mobile
Look up keyword
Like this
1Activity
×
0 of .
Results for:
No results containing your search query
P. 1
Bridging the transgenerational gap with epigenetic memory (March 2013)

Bridging the transgenerational gap with epigenetic memory (March 2013)

Ratings:

4.0

(1)
|Views: 848|Likes:
Published by slartibartfastibast
https://www.sciencedirect.com/science/article/pii/S0168952512002120
https://www.sciencedirect.com/science/article/pii/S0168952512002120

More info:

Categories:Types, Research
Published by: slartibartfastibast on Apr 07, 2013
Copyright:Attribution Non-commercial

Availability:

Read on Scribd mobile: iPhone, iPad and Android.
download as PDF, TXT or read online from Scribd
See More
See less

12/03/2013

pdf

text

original

 
FeatureReview 
Bridging
 
thetransgenerationalgapwith
 
epigenetic
 
memory
JanaP.Lim
1,2
andAnneBrunet
1,2,3
1
Department
 
of 
 
Genetics,
 
Stanford
 
University
 
School
 
of 
 
Medicine,
 
Stanford,
 
CA
 
94305,
 
USA
2
Neurosciences
 
Program,
 
Stanford
 
University
 
School
 
of 
 
Medicine,
 
Stanford,
 
CA
 
94305,
 
USA
3
Glenn
 
Laboratories
 
for
 
the
 
Biology
 
of 
 
Aging,
 
Stanford,
 
CA
 
94305,
 
USA
It
 
is
 
textbook
 
knowledge
 
that
 
inheritance
 
of
 
traits
 
isgoverned
 
by
 
genetics,
 
and
 
that
 
the
 
epigenetic
 
modifica-tionsan
 
organism
 
acquires
 
are
 
largely
 
reset
 
betweengenerations.
 
Recently,
 
however,
 
transgenerational
 
epi-genetic
 
inheritance
 
has
 
emerged
 
as
 
a
 
rapidly
 
growingfield,
 
providing
 
evidence
 
suggesting
 
that
 
some
 
epige-netic
 
changes
 
result
 
in
 
persistent
 
phenotypes
 
acrossgenerations.
 
Here,
 
we
 
survey
 
some
 
of
 
the
 
most
 
recentexamples
 
of
 
transgenerational
 
epigenetic
 
inheritancein
 
animals,
 
ranging
 
from
 
Caenorhabditis
 
elegans
 
tohumans,
 
and
 
describe
 
approaches
 
and
 
limitations
 
tostudying
 
this
 
phenomenon.
 
We
 
also
 
review
 
the
 
currentbody
 
of
 
evidence
 
implicating
 
chromatin
 
modificationsand
 
RNA
 
molecules
 
in
 
mechanisms
 
underlying
 
this
 
un-conventional
 
mode
 
of
 
inheritance
 
and
 
discuss
 
its
 
evolu-tionary
 
implications.Unconventional
 
mode
 
of
 
inheritance
Heredity 
 
is
 
overwhelmingly 
 
acknowledged
 
to
 
be
 
governedby 
 
the
 
laws
 
of 
 
Gregor
 
Mendel,
 
with
 
genes
 
as
 
the
 
primary templates
 
of 
 
inherited
 
information.
 
However,
 
an
 
increas-ingnumber
 
ofexceptions
 
to
 
the
 
rules
 
of 
 
genetic
 
inheritancehave
 
been
 
reported,
 
suggesting 
 
that
 
additional
 
layers
 
of information
 
are
 
also
 
transmitted.
 
During 
 
the
 
1920s,
 
inher-itance
 
of 
 
mating 
 
behavior
 
in
 
toads
 
was
 
reported
 
by 
 
PaulKammerer
 
[1],
 
although
 
this
 
study 
 
remains
 
controversial[2].
 
During 
 
the
 
1940s,
 
Conrad
 
Waddington
 
coined
 
the
 
term‘epigenetic’
 
and
 
described
 
inheritance
 
of 
 
wing 
 
patternsin
 
response
 
to
 
heat
 
shock 
 
in
 
 Drosophila
 
[4].
 
Shortly 
 
after, Alexander
 
Brink 
 
discovered
 
an
 
unconventional
 
mode
 
of inheritance
 
for
 
pigment
 
biosynthesis
 
in
 
plants
 
and
 
termedit
 
‘paramutation’
 
[5].The
 
discovery 
 
of 
 
parental
 
imprinting in
 
mammals
 
during 
 
the
 
1980s
 
provided
 
the
 
first
 
indicationthat
 
epigenetic
 
modifications,
 
such
 
as
 
DNA 
 
methylation,were
 
not
 
entirely 
 
erased
 
between
 
generations
 
and
 
couldunderlie
 
transgenerational
 
epigenetic
 
inheritance
 
 
was
 
also
 
around
 
this
 
time
 
that
 
several
 
cases
 
of 
 
transge-nerational
 
epigenetic
 
inheritance
 
were
 
reported
 
in
 
mice,for
 
both
 
exogenous
 
transgenes
 
and
 
endogenous
 
allelesaffecting 
 
coat
 
color
 
[12,13].Since
 
these
 
breakthroughreports,
 
additional
 
cases
 
of 
 
nongenetic
 
inheritance
 
havebeen
 
reported
 
inspecies
 
ranging 
 
from
 
worms
 
to
 
mammals,suggesting 
 
that
 
this
 
phenomenon
 
is
 
more
 
widespread
 
thanoriginally 
 
thought.
 
In
 
parallel,
 
a
 
growing 
 
body 
 
of 
 
work 
 
hasrevealed
 
that
 
exposure
 
of 
 
parents
 
to
 
environmental
 
stimulicould
 
affect
 
the
 
phenotype
 
of 
 
several
 
generations
 
of 
 
des-cendants,
 
suggesting 
 
that
 
changes
 
in
 
epigenetic
 
modifica-tions
 
induced
 
by 
 
environmental
 
stimuli
 
might
 
be
 
passed
 
ontodescendants
 
 via
 
the
 
gametes.
 
Importantly,
 
the
 
field
 
hasrecently 
 
made
 
significant
 
progress
 
in
 
garnering 
 
mechanis-tic
 
insight
 
into
 
the
 
processes
 
underlying 
 
transgenerationalepigenetic
 
inheritance,
 
by 
 
implicating 
 
specific
 
chromatinmodifications
 
and
 
noncoding 
 
RNA 
 
molecules.Inthis
 
review,
 
we
 
survey 
 
the
 
most
 
recent
 
examples
 
of epigenetic
 
inheritance
 
induced
 
by 
 
genetic
 
and
 
environmen-tal
 
perturbations
 
in
 
animals
 
(epigenetic
 
inheritance
 
inplants
 
has
 
been
 
reviewed
 
elsewhere
 
[14,15]).We
 
alsodiscuss
 
the
 
current
 
state
 
of 
 
progress
 
in
 
elucidating 
 
molec-ularmechanisms
 
of 
 
this
 
unconventional
 
mode
 
of 
 
inheri-tance,
 
primarily 
 
focusing 
 
on
 
chromatin
 
and
 
noncoding RNAs,
 
since
 
the
 
role
 
of 
 
DNA 
 
methylation
 
has
 
been
 
exten-sivelyreviewed
 
elsewhere
 
 
We
 
mostly 
 
focus
 
oninstances
 
of 
 
nongenetic
 
inheritance
 
that
 
persist
 
for
 
severalgenerations
 
(but
 
that
 
are
 
not
 
permanent),
 
because
 
persis-tence
 
over
 
multiple
 
generations
 
reduces
 
likelihood
 
of confounding 
 
factors,
 
such
 
as
 
maternal
 
effects
 
or
 
directexposure
 
of 
 
the
 
gametes
 
to
 
toxins.
 
We
 
also
 
discuss
 
theseimportant
 
limitations
 
to
 
our
 
understanding 
 
of 
 
the
 
mecha-nisms
 
underlying 
 
transgenerational
 
epigenetic
 
inheri-tance.
 
Finally,
 
we
 
reflect
 
on
 
the
 
potential
 
evolutionary implications
 
of 
 
this
 
previously 
 
underappreciated
 
mode
 
of inheritance.
Epigenetic
 
inheritance
 
induced
 
by
 
alterations
 
of
 
theparental
 
genome
Studying 
 
wild
 
type
 
descendants
 
of 
 
ancestors
 
with
 
muta-tions
 
in
 
specific
 
genomic
 
loci
 
has
 
revealed
 
that,
 
in
 
somecases,
 
phenotypes
 
characteristic
 
ofthe
 
mutant
 
ancestorsarestill
 
present
 
in
 
wild
 
type
 
descendants
 
1).
Transgenerational 
 
epigenetic 
 
inheritance 
 
of 
 
color 
 
and size 
 
in 
 
mice 
 Alterations
 
inthe
 
genome,
 
for
 
example
 
transcriptionalactivation
 
of 
 
a
 
chromosomal
 
element
 
and
 
retrotransposoninsertion,
 
were
 
shown
 
to
 
lead
 
to
 
transgenerational
 
epige-netic
 
inheritance
 
of 
 
Drosophila
 
eye
 
color
 
and
 
mousecoat
 
color
 
[12],respectively.
 
More
 
recently,
 
additional
Review
Correspondingauthor:
 Keywords:
transgenerational;epigeneticinheritance;chromatin;noncodingRNA;aging;fertility;metabolism;stressstimuli.
176
0168-9525/$seefrontmatter
ß
2013ElsevierLtd.Allrightsreserved.http://dx.doi.org/10.1016/j.tig.2012.12.008TrendsinGenetics,March2013,Vol.29,No.3
 
examples
 
of 
 
transgenerational
 
epigenetic
 
inheritance
 
in-duced
 
by 
 
alterations
 
of 
 
the
 
parental
 
genome
 
were
 
de-scribed
 
in
 
mice,
 
implicating 
 
RNA 
 
in
 
this
 
phenomenon[23–25].
 
In
 
the
 
first
 
study,
 
mice
 
with
 
an
 
insertion
 
of 
 
LacZinto
 
the
 
 Kit
 
gene
 
gave
 
rise
 
to
 
genetically 
 
wild
 
type
 
offspring that
 
still
 
exhibited
 
the
 
tail
 
and
 
paw
 
color
 
phenotype
 
char-acteristic
 
of 
 
 Kit
 
mutants
 
for
 
at
 
least
 
two
 
generations
 
[23].Genetically 
 
wild
 
type
 
descendants
 
of 
 
ancestors
 
that
 
hadthe
 
 Kit
 
mutant
 
phenotype
 
showed
 
an
 
altered
 
pattern
 
of 
 
 Kit
RNAexpression,
 
with
 
RNA 
 
molecules
 
of 
 
shorter
 
size
 
inbrain
 
and
 
testis
 
[23].Microinjection
 
of 
 
RNA 
 
from
 
hetero-zygous
 
mutant
 
animals
 
into
 
one-cell
 
embryos
 
was
 
suffi-cient
 
to
 
recapitulate
 
the
 
mutant
 
phenotype
 
in
 
the
 
following generation
 
[23].Collectively,
 
these
 
data
 
suggest
 
that
 
dis-ruption
 
of 
 
a
 
genomic
 
locus
 
in
 
parents
 
(in
 
this
 
case
 
by 
 
LacZinsertion)
 
leads
 
to
 
abnormal
 
RNA 
 
production
 
in
 
sperm,which
 
may 
 
be
 
transmitted
 
in
 
a
 
transgenerational
 
mannerfor
 
at
 
least
 
two
 
generations.
 
However,
 
the
 
exact
 
mecha-nisms
 
underlying 
 
this
 
epigenetic
 
memory 
 
are
 
still
 
unclear.Theimportance
 
of 
 
RNAin
 
epigenetic
 
inheritanceinmicewas
 
bolstered
 
by 
 
twoexamples
 
of 
 
transgenerationalinheri-tanceof 
 
cardiachypertroph
 
and
 
organismal
 
growth
 
[24,25].Injection
 
of 
 
fertilizedeggs
 
withRNAsandmiRNAs
 
target-ingcyclin-dependent
 
kinase
 
9
 
(
Cdk9
),a
 
regulator
 
ofcardiacgrowth,
 
resulted
 
incardiac
 
hypertrophy 
 
in
 
thenextgenera-tions[24].
 
Furthermore,
 
injection
 
of 
 
miR-124
,
 
a
 
miRNA normally 
 
expressed
 
in
 
thebrainandinvolved
 
incentralnervoussystemdevelopment,
 
intofertilized
 
eggs
 
resultedinprogenythatexhibiteda
 
30%largerthannormalbodysize[25].
 
This
 
‘giant’phenotypepersisted
 
untiltheF2
 
genera-tion,afterwhich
 
thebody 
 
size
 
of 
 
thedescendants
 
revertedback 
 
to
 
normal.
 
These
 
studies
 
suggest
 
thatRNA-mediatedepigenetic
 
phenomena
 
underlie
 
theinheritance
 
of 
 
selectphenotypes.Whysome
 
RNAshave
 
a
 
potential
 
for
 
transge-nerationaleffects
 
whereas
 
others
 
do
 
notis
 
still
 
unclear.Nongenetic
 
inheritanceof 
 
traits
 
such
 
as
 
organand
 
animalsize
 
may 
 
have
 
crucial
 
implicationsfor
 
theetiologyofhumanhypertrophic
 
cardiac
 
myopathy 
 
andobesity.
Transgenerational 
 
epigenetic 
 
inheritance 
 
of 
 
fertility 
 
and longevity 
 
in 
 
C.
 
elegans
Examples
 
of 
 
transgenerational
 
epigenetic
 
inheritance
 
in-duced
 
by 
 
alterations
 
of 
 
the
 
parental
 
genome
 
were
 
alsorecently 
 
described
 
in
 
the
 
nematode
 
Caenorhabditis elegans
.
C.
 
 elegans
 
is
 
a
 
powerful
 
model
 
system
 
for
 
thestudy 
 
of 
 
epigenetic
 
memory 
 
given
 
its
 
rapid
 
generation
 
timeand
 
amenability 
 
for
 
controlling 
 
many 
 
environmental
 
andgenetic
 
 variables.
 
Transgenerational
 
epigenetic
 
inheri-tance
 
of 
 
sterility 
 
and
 
longevity 
 
have
 
both
 
been
 
reported,and
 
involve
 
similar
 
histone
 
modifications
 
[26,27].First,mutants
 
of 
 
spr-5
,
 
one
 
of 
 
the
 
worm
 
orthologs
 
of 
 
the
 
lysine-specific
 
histone
 
demethylase
 
1A 
 
(LSD1/KDM1),
 
whichdemethylates
 
the
 
histone
 
3
 
lysine
 
4
 
dimethyl
 
mark (H3K4me2)
 
[28],exhibit
 
progressive
 
decreased
 
brood
 
sizebeginning 
 
in
 
the
 
first
 
generation
 
and
 
progressive
 
progeny sterility 
 
starting 
 
around
 
generation
 
20
 
[26].The
 
fertility 
 
of severely 
 
sterile
 
generations
 
was
 
rescued
 
byintroducinone
 
wild
 
type
 
copy 
 
of 
 
spr-5
 
for
 
one
 
generation
 
[26],indicat-ingthat
 
this
 
is
 
sufficient
 
to
 
induce
 
epigenetic
 
resetting.Interestingly,
 
accumulation
 
of 
 
H3K4me2
 
and
 
misregula-tion
 
of 
 
spermatogenesis
 
genes
 
is
 
observed
 
in
 
the
 
primordialgerm
 
cells
 
(PGC)
 
of 
 
spr-5
 
mutants
 
[26].Indeed,
 
it
 
has
 
beenrecently 
 
shown
 
that
 
H3K4me2
 
increases
 
throughout
 
theentire
 
germline
 
of 
 
spr-5
 
mutants
 
[28].Together,
 
theseresults
 
suggest
 
that
 
failure
 
to
 
reset
 
H3K4me2
 
marks
 
atselect
 
germline
 
genes
 
in
 
the
 
PGCs
 
results
 
in
 
progressivetransgenerational
 
sterility.More
 
recently,
 
the
 
first
 
example
 
of 
 
transgenerationalepigenetic
 
inheritance
 
of 
 
longevity 
 
was
 
described
 
[27].Genetically 
 
wild
 
type
 
descendants
 
from
 
ancestors
 
thatare
 
mutant
 
for
 
members
 
of 
 
the
 
COMPASS
 
H3K4
 
methyla-tioncomplex
 
display 
 
increased
 
lifespan
 
for
 
up
 
to
 
threegenerations.
 
The
 
COMPASS
 
complex
 
comprises
 
 ASH-2,WDrepeat-containing 
 
protein
 
5
 
(WDR-5)
 
and
 
SET-2
 
inworms.
 
This
 
complex
 
is
 
conserved
 
across
 
species,
 
andcatalyzes
 
the
 
trimethylation
 
of 
 
lysine
 
4
 
ofhistone
 
H3(H3K4me3)
 
[29],a
 
chromatin
 
modification
 
commonly 
×
+/+
 
 –/–+/–+/+ +/F3, F4, F5…
×
+/++/+ +/F1F2P0
(a)(b)
GeneƟcallywild type,phenotypicallymutant+/+
 
 –/–+/–+/+
 
 –/–+/–
 
+/–GeneƟcallywild type,phenotypicallymutantF3, F4, F5…
×
Self ferƟlizaƟonF2F1P0
TRENDS in Genetics 
Figure1
.
 
Transgenerationalepigeneticinheritanceinducedbygeneticmodificationinancestors.
(a
)
 
Crossingschemeusedinrodentstudiestogenerategeneticallywildtypeprogenyfromamutantancestor.
(b)
Crossingschemeusedinwormstudiestogenerategeneticallywildtypeprogenyfromamutantancestor.TheF1generationarisesfrommatingbetweenahermaphroditeandmale.TheF2generationarisesfromtheselffertilizationofF1hermaphrodites.Key:red,wildtype;blue,mutant;gray,unknownphenotype.
Review
Trends 
 
in 
 
Genetics 
 
March
 
2013,
 
Vol.
 
29,
 
No.
 
3
177
 
associated
 
withactivelytranscribed
 
genes[30].
 
Deficiency in
 
COMPASS
 
complexmembers
 
extends
 
lifespan
 
in
 
a
 
man-nerthatdepends
 
on
 
thepresence
 
of 
 
a
 
functional
 
germline[31].Geneticallywildtype
 
descendants
 
from
 
a
 
crossbe-tween
 
wild
 
type
 
males
 
andhermaphroditeswithmutationsinthe
wdr-5
 
or
 
set-2
geneswere
 
longlivedfor
 
up
 
to
 
threegenerationscompared
 
withdescendants
 
from
 
purewildtype
 
ancestors[27].
 
The
 
long 
 
lifespan
 
of 
 
thedescendantsis
 
dependent
 
on
 
theH3K4me3
 
demethylase
 
retinoblastomabindingprotein
 
related
 
2
 
(RBR-2)andrequires
 
a
 
function-inggermline[27].
 
This
 
suggests
 
thatlongevityof 
 
wild
 
typedescendants
 
froma
 
cross
 
betweenmutant
 
ancestorsandwild
 
type
 
worms
 
is
 
unlikelyto
 
be
 
dueto
 
an
 
extraneousmutation
 
present
 
in
 
theinitial
 
strain.Transgenerationalinheritanceof 
 
longevityappeared
 
to
 
be
 
relativelyspecifictomembers
 
of 
 
theCOMPASS
 
complex,
 
because
 
manipulationofother
 
longevity-promoting 
 
pathways,
 
such
 
as
 
theinsulinsignaling 
 
andmitochondrialpathways,
 
or
 
other
 
chromatinregulators,did
 
notshow
 
a
 
transgenerationalinheritance
 
of long 
 
life[27].
 
These
 
findings
 
show
 
thatmanipulation
 
of specific
 
chromatin
 
modifiers
 
in
 
parents
 
canhave
 
lasting effects
 
on
 
complex
 
traits
 
of 
 
offspring.
 
It
 
is
 
interesting 
 
to
 
notethat
 
both
 
casesof 
 
transgenerationalinheritance[26,27]involve
 
theregulationof 
 
H3K4
 
methylationin
 
thegermline,suggesting 
 
thatthishistone
 
mark 
 
is
 
particularlyimportantfor
 
themechanismof 
 
epigenetic
 
memory.Together,
 
these
 
data
 
describe
 
instances
 
where
 
initialperturbation
 
of 
 
the
 
genome
 
of 
 
an
 
ancestor
 
can
 
result
 
intransgenerational
 
epigenetic
 
inheritance
 
ofa
 
 variety 
 
of traits.
 
These
 
observations
 
also
 
raise
 
the
 
intriguing 
 
possi-bility 
 
that
 
environmental
 
stimuli
 
that
 
perturb
 
RNA 
 
orchromatin
 
states
 
could
 
also
 
affect
 
phenotypes
 
of 
 
descen-dants
 
for
 
multiple
 
generations.
 
However,
 
the
 
prevalenceand
 
specificity 
 
of 
 
this
 
epigenetic
 
mode
 
of 
 
inheritance
 
is
 
stillunknown.
 
Furthermore,
 
the
 
exact
 
sequence
 
and
 
nature
 
of events
 
by 
 
which
 
initial
 
mutations
 
in
 
chromatin
 
modifiersinancestors
 
lead
 
to
 
relatively 
 
persistent
 
phenotypechanges
 
in
 
wild
 
type
 
descendants
 
is
 
not
 
known,
 
and
 
isdiscussed
 
further
 
below,
 
in
 
the
 
mechanism
 
section.
Epigenetic
 
inheritance
 
induced
 
by
 
metabolic
 
changes
 
inparents
Interestingly,
 
epigenetic
 
inheritance
 
canalsobe
 
induced
 
by environmentalchanges
 
in
 
parents.
 
The
 
pastfew
 
yearshaveseena
 
urryo
 
reports
 
on
 
theinheritance
 
of 
 
acquiredmetabolic
 
phenotypes
 
resultingfrom
 
over-
 
or
 
undernutri-tionin
 
parents.
 
To
 
avoidpotential
 
confounds
 
of 
 
in
 
utero
 
andaltered
 
maternalcaretaking,studies
 
haveinvestigatedtransgenerationalinheritanceof 
 
metabolic
 
physiology throughthepaternal(Figure
2a)or
 
thematernal(Figure
2b)lineage.
 
In
 
such
 
schemes,
 
thegametes
 
of 
 
theP0
 
fatheror
 
theF1
 
motheraredirectl
 
exposed
 
to
 
theenvironmentalstimulus,
 
which
 
may 
 
alterthegenomeinways
 
thatcould
 
be
 
transmittedto
 
theF1
 
or
 
F2
 
offspring,respectively.Thus,
 
studyingtheF2
 
generationfrom
 
malesor
 
F3
 
generationfrom
 
females
 
provides
 
a
 
way 
 
to
 
distinguishdirect
 
exposure
 
fromepigeneticinheritance(Figure
2).
Overfeeding 
Exposure
 
to
 
a
 
chronic
 
high-fat
 
diet
 
in
 
rat
 
fathers
 
resultedin
 
impaired
 
insulin
 
metabolism
 
and
 
pancreatic
 
cell
 
geneexpression
 
in
 
female
 
F1
 
offspring 
 
[32].Female
 
offspring from
 
fathers
 
fed
 
a
 
high
 
fat
 
diet
 
mated
 
with
 
mothers
 
fed
 
acontrol
 
diet
 
exhibited
 
an
 
increase
 
in
 
blood
 
glucose
 
in
 
theglucose
 
tolerance
 
test
 
and
 
a
 
decrease
 
in
 
insulin
 
secretioncompared
 
with
 
offspring 
 
with
 
both
 
parents
 
fed
 
a
 
controldiet
 
[32].Microarray 
 
analysis
 
of 
 
islet
 
cells
 
from
 
femaleoffspring 
 
of 
 
fathers
 
fed
 
a
 
high-fat
 
diet
 
uncovered
 
genesinvolved
 
in
 
a
 
range
 
of 
 
pathways,
 
including 
 
insulin
 
andglucose
 
metabolism
 
as
 
well
 
as
 
mitogen-activated
 
protein
Diet,stress
×
+/++/++/++/+
Diet,stress
Normal environment,altered phenotypeNormal environment,altered phenotype
×
+/+F2F1P0
(a)(b)
×
+/++/++/+
×
+/++/+
×
+/+F2F1P0F3+/+
 
,ress
ormalaltere
×
 /+ /+ /+environment,phenotype
×
 /+
TRENDS in Genetics 
Figure2
.
 
Transgenerationalepigeneticinheritanceinducedbyenvironmentalmanipulationsinancestors.
(a
)
 
Strategyusedtogenerateprogenyfromapaternalancestorsubjecttoanenvironmentalperturbation.Thisschememinimizesmaternaleffectsinorganismsthatrequiresignificantmaternalcareduringdevelopment.
(b
)
 
Schemeusedtogenerateprogenyfromamaternalancestorsubjecttoanenvironmentalperturbation.Thisschemeallowsforthestudyof transgenerationaleffectsinducedbyaninitialchangeinmaternalenvironment,butminimizescrypticmaternaleffects.Key:blue,normalphenotype;green,alteredphenotyperesultingfromaperturbationtotheancestralenvironment.
Review
Trends 
 
in 
 
Genetics 
 
March
 
2013,
 
Vol.
 
29,
 
No.
 
3
178

You're Reading a Free Preview

Download
/*********** DO NOT ALTER ANYTHING BELOW THIS LINE ! ************/ var s_code=s.t();if(s_code)document.write(s_code)//-->